University of Southern California Dissertations and Theses

How emotional arousal influences memory and learning in younger and older adults

(USC Thesis Other)

How emotional arousal influences memory and learning in younger and older adults

PDF

Download a page range

Download transcript

Copy asset link

Request this asset

Transcript (if available)

Content

HOW EMOTIONAL AROUSAL INFLUENCES MEMORY AND LEARNING
IN YOUNGER AND OLDER ADULTS

by

Kaoru Nashiro

________________________________________________________

A Dissertation Presented to the
FACULTY OF THE USC GRADUATE SCHOOL
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfillment of the
Requirements for the Degree
DOCTOR OF PHILOSOPHY
(GERONTOLOGY)

August 2012

Copyright 2012 Kaoru Nashiro

ii

DEDICATION
This dissertation is dedicated to my family, friends and colleagues who taught me
the value of education and hard work. Their moral support and encouragement helped
make this work possible.
iii

ACKNOWLEDGMENTS
I am grateful to my dissertation committee advisors, Dr. Mara Mather, Dr.
Margaret Gatz, Dr. Bob Knight and Dr. Gerald Davison. I would like to offer a sincere
thank you to Dr. Mather for her excellent mentorship and guidance throughout my
graduate student career. Thank you to Dr. Gatz for careful reading and valuable feedback
for improving this study. Thank you to Dr. Knight for critiquing my research and
providing constructive comments and suggestions. A special and warm thank you to Dr.
Davison for stepping in to serve on my committee at extremely short notice and for
providing great insight into my research. This work was supported by grants from the
National Institute on Aging (R01AG025340, K02AG032309 and 5T32AG000037).

iv

TABLE OF CONTENTS
Dedication ii
Acknowledgments iii
List of Tables v
List of Figures vi
Abstract vii
Introduction 1
Chapter 1: How Emotional Arousal Affects Associative Memory in Younger 4
and Older Adults
Chapter 2: Both Younger and Older Adults Have Difficulty Updating 50
Emotional Memories
Chapter 3: Age-related Similarities and Differences in Brain Activity 58
During Emotional vs. Non-emotional Memory Updating
Conclusion 88
References 92

v

LIST OF TABLES
Table 1: Proportion of Items Recalled, and Location and Pair Memory 24
Accuracy for Arousing (Positive and Negative) vs. Neutral Items in
Association vs. Non-association Conditions

Table 2: Item and Location Memory Accuracy for Neutral, Negative and 47
Positive Items

Table 3: Item Hit and False Alarm (FA) Rates for Arousing (Negative and 48
Positive) and Non-arousing Items in Experiment 3
Table 4: Brain Activity Showing Significant Differences between Conditions 84
during Reversal Learning in Younger and Older Adults

Table 5: Brain Regions Showing Negative Connectivity with the Left Amygdala 86
across Groups

Table 6: Brain Regions Showing Age-related Differences in Positive Connectivity 87
with the Parietal Cortex
vi

LIST OF FIGURES
Figure 1: Proportion of Items Recalled and Location and Pair Memory 25
Accuracy

Figure 2: Location Memory Accuracy for Arousing and Non-arousing Items 49

Figure 3: Picture-Location Association Memory 57

Figure 4: Experimental Procedure 78

Figure 5: Brain Regions Showing Differences between Conditions 80
during Reversal Learning across Groups

Figure 6: Brain Activity in the Left Lateral OFC and the Left Amygdala 81
during Reversal Learning across Conditions

Figure 7: Brain Regions Showing Negative Connectivity with the Left Amygdala 82
across Groups

Figure 8: Brain Activity in the Parietal Cortex Showing Age-related Differences 83
in the Neutral Condition
vii

ABSTRACT
Older adults commonly experience difficulty remembering associative
information. This can lead to a number of negative health outcomes and affects their
quality of life. Thus, it is important to try to reduce the impact of the decline by
understanding what factors might influence their memory performance. Given that
emotional processing is well preserved in normal aging, it is possible that emotion
modulates associative memory in a similar way in younger and older adults. The current
study investigated this possibility by using behavioral and functional MRI (fMRI)
methods. The behavioral results revealed that emotional arousal enhances or impairs
associative memory depending on novelty of the items in both younger and older adults.
The fMRI results suggested that both age groups showed similar patterns of activation in
the amygdala and the frontopolar OFC regions. However, age-group differences were
found when associative learning does not involve emotion; older adults showed greater
parietal cortex activity than did younger adults, possibly reflecting compensatory
recruitment. This study provides important new information about how emotional
arousal influences associative learning in older adults, which will help us develop
strategies to improve associative learning in general.
1

INTRODUCTION
Memory decline is commonly associated with aging and can lead to a number of
other negative health outcomes. For example, age-related memory impairment is related
to a greater decline in instrumental activities of daily living (Tomaszewski Farias et al.,
2009), hearing loss (Lin et al., 2011), and fear of falling (Uemura et al, 2012).
Furthermore, concerns about memory decline are associated with depression and anxiety
(Montejo, Montenegro, Fernandez, & Maestu, 2012), lower activities of daily living, and
poor quality of life (Mol et al., 2007; Montejo, Montenegro, Fernandez, & Maestu, 2012).
Thus, it is important to understand how to minimize age-related memory decline and
what factors might influence memory performance in older adults.
One type of memory particularly affected by age is associative memory (or
memory binding
1
). Associative memory is the ability to remember various features of an
object, person, or event together as a coherent whole, which is an essential component of
episodic memory. For example, older adults commonly experience difficulty
remembering where they may have left their personal belongings, such as car keys and
eyeglasses, as a result of impaired recall of associations between items and locations. A
number of laboratory studies have demonstrated that older adults have an associative
memory deficit compared with their younger counterparts (Chalfonte & Johnson, 1996;
Kessels, Hobbel, & Postma, 2007; Mitchell, Johnson, Raye, Mather, & D'Esposito, 2000;
Naveh-Benjamin, 2000; Pezdek & Hartman, 1983). This is consistent with the
associative deficit hypothesis (Naveh-Benjamin, 2000), which postulates that an age-
related decline in episodic memory is, in part, due to impairments in associative memory.

1
“Associative memory” and “memory binding” are used interchangeably throughout this paper,
as I am unable to change the wording that has been used in previous publications.
2

Neuroimaging studies suggest that the prefrontal cortex and the hippocampal-medial
temporal region are critical for associative memory (Achim & Lepage, 2005; Davachi &
Wagner, 2002; Kramer et al., 2005; Olson, Page, Moore, Chatterjee, & Verfaellie, 2006;
Ryan & Cohen, 2004) and these regions decline in volume in normal aging (Bartzokis et
al., 2001; Raz et al., 2005). Furthermore, previous studies show reduced hippocampal
activity in older adults compared with younger adults during stimuli presentation
conditions that elicit or require associative learning (Chee et al., 2006; Goh et al., 2007;
Mitchell, Johnson, Raye, & D'Esposito, 2000).
However, not all brain regions are affected by age to the same extent. The
amygdala, one of the emotional centers of the brain, shows less volumetric decline with
age than do most other brain regions (Allen, Bruss, Brown, & Damasio, 2005).
Postmortem measurements based on histological staining reveal no significant effect of
age on amygdala volume (Brabec et al., 2010). Consistent with these neuroimaging
findings, behavioral evidence suggests that emotional processing is well preserved in
normal aging. For instance, the ability to detect emotionally arousing stimuli is relatively
stable with age (Leclerc & Kensinger, 2008), and the effects of emotional arousal on item
memory remain intact in older adults (Denburg, Buchanan, Tranel, & Adolphs, 2003).
Furthermore, younger and older adults exhibit similar skin conductance responses to
emotionally arousing stimuli (Denburg et al., 2003; Neiss, Leigland, Carlson, &
Janowsky, 2009).
Although emotion and memory rely on different brain structures, these regions
can nevertheless also interact with each other, which results in enhancing or impairing
memory performance. Given that emotional processing is preserved in normal aging, it
3

seems possible that emotion modulates associative memory similarly in younger and
older adults; however, previous studies have provided mixed results. Thus, this
dissertation examines the interactions between emotion and associative memory in older
adults as compared with younger adults. Chapter 1 (Nashiro & Mather, 2011a, 2011b)
investigates whether emotional arousal can enhance associative memory for new items in
older adults, as previously seen in younger adults. Chapter 2 (Nashiro, Sakaki, Huffman,
& Mather, in press) examines whether emotional arousal has impairing effects on
associative memory for previously encountered items (as opposed to new items) in older
adults, as previously seen in younger adults. In Chapter 3 (Nashiro Sakaki, Nga, &
Mather, in preparation), a functional MRI method was used to investigate whether there
are different brain mechanisms underlying emotional versus neutral memory updating in
older adults, as has previously been seen in younger adults.
4

CHAPTER 1: HOW EMOTIONAL AROUSAL INFLUENCES YOUNGER AND
OLDER ADULTS’ ASSOCIATIVE MEMORY

1.1 How Arousal Affects Younger and Older Adults' Memory Binding
2

Kaoru Nashiro and Mara Mather

Memory binding is an essential component of episodic memory; it allows people to
remember a combination of features of an object, a person, or an event. For example, if
you witness a car accident, your ability to bind disparate elements of an event together
will determine whether you remember which driver was in each car. How does having an
emotionally arousing component as part of an event affect memory binding? Recent
laboratory studies indicate that the emotional arousal elicited by a stimulus item (such as
a picture or word) can either enhance or impair later memory for the features or context
associated with that item. For instance, a number of studies have found that memory for
the color or location of emotional items is better than memory for the color or location of
neutral items (Doerksen & Shimamura, 2001; Hadley & Mackay, 2006; Kensinger &
Corkin, 2003; MacKay & Ahmetzanov, 2005; Mather, Gorlick, & Nesmith, 2009; Mather
& Nesmith, 2008). However, other studies have found that memory for other items
shown near emotionally arousing items or memory for which a task was performed on
emotionally arousing items is poorer than memory for these types of associated
information for neutral items (Anderson & Shimamura, 2005; Cook, Hicks, & Marsh,
2007; Kensinger & Schacter, 2006).

2
This is an already published paper with minor modifications in the introduction and discussion
sections in order to fit within the organization of the dissertation.
5

The effect of arousal on two types of memory binding
To account for the discrepant effects of arousal on different aspects of memory
binding, Mather (2007) proposed an object-based memory-binding framework.
According to this framework, whether or not arousal enhances memory binding depends
on whether the features to be bound are from the same target item (e.g., a car and its
color) or from distinct items (e.g., a car and a pedestrian). When a target item is
emotionally arousing, the arousal enhances the former type of binding (within-item
memory binding) but does not improve the latter (between-item memory binding). This
discrepancy is due to the way arousal influences attention allocation. Focused attention
on an object is necessary to perceive its various features as a coherent whole (Treisman,
1998). When an arousing object attracts attention, it leads to enhanced memory binding
of the features that are the focus of attention, which include all of the features that
comprise the object itself. However, arousing objects may also reduce attention to the
broader scope of the scene and interrelationships between the arousing object and other
nearby objects, impairing between-item memory binding.
Aging and memory binding
The studies described previously that revealed effects of arousal on memory
binding were all conducted with younger adults. However, it remains unclear whether
arousal has the same effects on memory binding in older adults. Previous studies
examining the effects of emotional arousal on memory (but not memory binding) suggest
that the effects remain similar in normal aging (Denburg et al., 2003; Kensinger, Brierley,
Medford, Growdon, & Corkin, 2002; Kensinger, Gutchess, & Schacter, 2007). This
emotion-enhanced memory among older adults is consistent with findings that the
6

amygdala, one of the emotional centers of the brain, shows relatively little decline in
normal aging (for a review, see Mather, 2004). Despite an overall decline in memory
performance with age, both younger and older adults show significantly higher
activations in the amygdala for emotional stimuli than for neutral stimuli (e.g., Mather et
al., 2004).
Unlike the relative similarities across age groups in the effects of arousal on
memory, some recent studies have revealed age by valence interactions in memory, such
that a smaller proportion of what older adults remember tends to consist of negative
information than for younger adults (Charles, Mather, & Carstensen, 2003; Kensinger &
Schacter, 2008; Mather & Carstensen, 2003; Mather & Knight, 2005; Thomas & Hasher,
2006; Tomaszczyk, Fernandes, & MacLeod, 2008). Of particular relevance for our
hypothesized link between attention and the effects of arousal on memory binding, older
adults tend to spend less time looking at negative stimuli and more time looking at
positive stimuli than younger adults (Isaacowitz, Wadlinger, Goren, & Wilson, 2006a,
2006b; Knight et al., 2007; Mather & Carstensen, 2003; Rosler et al., 2005). One
possibility is that this might lead to less effective memory binding for negative than
positive stimuli among older adults. However, previous findings revealed that although
the amount of time a younger adult looked at a neutral or emotional picture predicted
their recognition accuracy for that picture, it did not predict their picture-location
memory accuracy (Mather & Nesmith, 2008). Thus, what seems more critical than total
study time for the arousal-enhanced location memory is the initial context encoding
strength (Malmberg & Shiffrin, 2005). Given that both older and younger adults are most
likely to look first at emotionally arousing pictures, regardless of their valence (Knight et
7

al., 2007), it seems that the effects of arousal on picture-location binding should be
similar across positive and negative stimuli for older adults. In this study, our main focus
was to examine the effects of arousal on memory binding.
In contrast to the relative similarities across age groups in the effects of arousal on
memory, there are clear differences in the overall effectiveness of memory binding. A
number of studies using neutral items as stimuli have suggested that older adults
compared with younger adults have deficits in within-item memory binding (Chalfonte &
Johnson, 1996; Cowan, Naveh-Benjamin, Kilb, & Saults, 2006; Kessels et al., 2007;
Naveh-Benjamin, 2000; Naveh-Benjamin, Guez, Kilb, & Reedy, 2004; Naveh-Benjamin,
Guez, & Shulman, 2004). Mitchell, Johnson, Raye, Mather, and D'Esposito (2000) found
that older adults’ memory binding impairment was not the result of poor item or feature
memory per se; rather, they have difficulty remembering item-feature combinations. To
test this, they presented drawings of different objects in various locations on the computer
screen. Each participant completed several blocks of trials. For each block, younger and
older participants were instructed to either remember 1) only which objects were
presented, 2) only in which location objects appeared or 3) the combination of objects
and their locations, and were only tested on the information that they were instructed to
study. Compared with younger adults, older adults performed significantly worse on the
combination task, whereas the two groups performed similarly on the first two single-
feature tasks (see also Hartman & Warren, 2005).
Neuroimaging studies provide further evidence for older adults’ binding deficit.
The prefrontal cortex and the hippocampal-medial temporal region are critical for
memory and memory binding (Achim & Lepage, 2005; Davachi & Wagner, 2002;
8

Kramer et al., 2005; Olson et al., 2006; Ryan & Cohen, 2004). These regions decline in
volume in normal aging (Bartzokis et al., 2001; Raz et al., 2005) and show less memory-
related activity in the hippocampus during memory encoding and retrieval tasks among
older adults than among younger adults (Daselaar, Fleck, Dobbins, Madden, & Cabeza,
2006; Grady et al., 1995). More direct evidence of binding deficits comes from studies
showing reduced hippocampal activity in older adults compared with younger adults
during stimuli presentation conditions that elicit or require memory binding (Chee et al.,
2006; Goh et al., 2007; Mitchell, Johnson, Raye, & D'Esposito, 2000). Likewise,
whereas younger adults show more left lateral prefrontal cortex activation when given a
memory test about the previous format and location of items than when given an old-new
memory test for the items themselves, older adults do not show this increased prefrontal
activity during the source judgment task (Mitchell, Raye, Johnson, & Greene, 2006).
Older adults also show deficits in between-item memory binding for neutral items
(Kilb & Naveh-Benjamin, 2007; Provyn, Sliwinski, & Howard, 2007). For example,
Naveh-Benjamin (2000) conducted a series of experiments investigating age differences
in memory for pairs of distinct items (word-nonword pairs) and found that older adults
have deficits in remembering item-item associations even when they have relatively
intact memory for individual items themselves. Another study (Naveh-Benjamin, Brav,
& Levy, 2007) also showed that older adults did not remember pairs of items as well as
did their younger counterparts. However, it is important to note that this deficit was
reduced when older adults were instructed to use effective strategies for making
connections between two items. In the current experiment, we explored the possibility
that strategy use improves memory binding.
9

In summary, evidence from both behavioral and neuroimaging studies has
suggested that older adults have deficits in within- and between- item memory binding
for neutral items. However, it is not clear whether age-related memory binding deficits
would be reduced for emotionally arousing materials, and whether the effects might vary
depending on the type of memory binding. Given the theoretical reasons to think that the
effects of arousal vary for different types of memory binding (Mather, 2007) and the fact
that both types of binding may occur simultaneously in real life, we used an encoding
paradigm in which participants were given the opportunity to make both types of
associations at the same time (picture-location and picture-nearby object binding). Thus,
the current study examined age differences in whether arousing components of stimuli
enhance 1) memory for items, 2) within-item memory binding, 3) and between-item
memory binding; and 4) whether strategy use improves both types of memory binding.
Experiment 1
Method
Participants
We recruited 24 undergraduates (M
age
=20.17, age range 18-29, 11 males, 13
females, M
education
=13.56) and 24 older adults over 65 years old from various retirement
communities (M
age
=77.08, age range 65-89, 6 males, 17 females, M
education
=14.75). The
younger participants received course credit for their undergraduate Psychology classes,
and older participants received monetary compensation for their participation. The
experiments were conducted using a laptop at either at participants’ homes, senior
centers, or in our laboratory.
10

Materials
We used 64 pictures from the International Affective Picture System (IAPS;
Lang, Bradley, & Cuthbert, 1999) and from outside sources, and 32 abstract shapes as
stimuli. The pictures consisted of matched pairs of neutral and arousing pictures that
were similar in appearance, complexity, content and focus of interest (for examples, see
Mather & Nesmith, 2008). Each participant only saw one version from each picture pair
so that if, for example, a participant saw a neutral version from picture pair 1, he or she
did not view the arousing version from that pair. Across participants, the two versions
were both presented with the same shape (e.g., the neutral and arousing versions from
picture pair 1 were both presented with shape 1); thus, each participant saw 32 picture-
shape pairs. Of these pairs, 16 were neutral images, and 16 were arousing images (8
positive and 8 negative). The number of stimuli was relatively small in order to avoid
potential floor effects in older adults’ memory. We also attempted to avoid ceiling
effects in younger adults by pretesting the number of stimuli. In a previous pilot study,
presenting 16 picture-shape pairs to younger adults resulted in a ceiling effect in a
location memory test whereas using 32 picture-shape pairs did not. We used PsyScope to
present the stimuli and record the participants’ responses. The screen was divided into 3
x 3 grids, with grid squares that were 300mm wide and 248mm high. The outer eight
areas were used to present the images. On each slide, one picture and one shape
simultaneously appeared in two of the eight cells. One image (either a picture or a shape)
was always located higher than the other. Each stimulus type appeared in each location
equally frequently.
11

Procedure
Participants first filled out the informed consent, demographic information, and a
brief emotion questionnaire consisting of 10 positive and 10 negative emotion words
(Positive and Negative Affect Schedule; Watson, Clark, & Tellegen, 1988).
Each participant then completed both an association and a non-association encoding
condition. In the association condition, participants were asked questions that required
them to make associations between each picture-shape pair. In the non-association
condition, the tasks did not require making associations between the images. Participants
were not informed about the upcoming memory tests; they were instructed to simply
observe stimuli and answer questions by pressing appropriate keys on the keyboard.
The two encoding conditions alternated in four blocks of trials (i.e., association,
non-association, association, and non-association); the order of which condition came
first was randomized. Each block had 16 trials; and participants saw all 32 picture-shape
pairs in the first two blocks, which were then repeated in the second two blocks (the
assignment of pictures to encoding conditions remained the same in the second
presentation). Which versions of the matched pictures were shown was counterbalanced
across participants, as was which encoding task was assigned to each picture-shape pair.
In the association condition, the following question appeared in the center of the
screen simultaneously with the presentation of a picture-shape pair: “is the picture higher
(H) or lower (L) than the shape?” The participants were instructed to indicate their
answers by pressing one of the keys marked “H” or “L”, at which point the next pair was
presented. In the non-association condition, a picture–shape pair was presented for 5000
ms during which the participants passively viewed the images. Immediately after the two
12

images disappeared, either a blue or red dot was randomly presented in one of the eight
outer cells of the screen with the question “is the dot blue or red?” in the center of the
screen. The participants were asked to indicate their answers by pressing one of the keys
labeled with a blue sticker or a red sticker.
Immediately after the encoding phase, participants completed three types of
memory tests in the following order; 1) a free recall test, 2) a location memory test, and
3) a pair memory test. In the recall test, we asked them to describe as many pictures as
they could remember in as much detail as possible. The location memory test assessed
within-item memory binding, or how well participants remembered combinations of
pictures and their direct features (location). We presented each of the 32 pictures in two
different locations, each of which had a number label. Participants were asked to indicate
in which location they believed the picture had appeared in during the encoding trials by
pressing one of the keys marked 1 through 8. The pair memory test assessed between-
item memory binding, or how well participants remembered picture-shape combinations.
We used a recognition test for the picture-shape combinations instead of a forced-choice
procedure, as we wanted to keep the locations of picture-shape pairs constant both at
encoding and at test (whether shapes were correctly paired with pictures or not at test) in
order to avoid allowing participants to use location of shapes as a determinant of pair
memory accuracy. To do so, we could not have included two pairs on the screen
simultaneously with both in their original locations. On each test trial, participants saw a
picture-shape pair and indicated whether each pair was a previously seen pair (there were
16 of these old pairs) or two previously seen items that had not been paired with each
13

other (there were another 16 of these foils) by pressing either the blue (paired) or the red
keys (not paired).
Participants provided arousal ratings for the pictures using 9 point scales (arousal:
1= least arousing to 9= most arousing). Three younger adults did not complete the
ratings due to time constraints. We categorized positive and negative pictures according
to IAPS’ evaluation into an arousing group and their matched pictures into a neutral
group. A 2 (group: younger and older) x 2 (arousal: arousing and neutral) ANOVA
revealed that there was a main effect of arousal, F(1,42)=374.13, MSE=.53, p<.001,
η
p
2
=.90. However, there was an interaction between group and arousal
(M
young
_
arousing
=6.51, SE=.26; M
young_neutral
=.3.02, SE=.23; M
old
_
arousing
=6.47, SE=.25;
M
old_neutral
=3.92, SE=.22), F(1,42)=9.08, MSE=.53, p<.01, η
p
2
=.18, suggesting that older
adults rated neutral pictures as more arousing than did younger adults. We took this
group difference into account in our analyses and will discuss the findings in the results
section.
Participants also gave valence ratings using a 9 point scale (valence: 1= most
negative, 5=neutral, 9= most positive). We excluded three older adults’ valence ratings
from our analyses, as they reported after the experiment that they used the valence rating
scales incorrectly. We also excluded all older subjects’ ratings for one of the pictures in
the negative category, which was a picture of a piece of pumpkin pie with a cockroach, as
most older participants reported that they failed to see the cockroach due to its small size
resulting in rating the picture as positive rather than negative (older adult valence rating
M=6.7). A 2 (Group) x 3 (valence: neutral, positive, negative) ANOVA revealed that
there was a main effect of valence, F(1,39)=449.85, MSE=.50, p<.001, η
p
2
=.92. As
14

expected, positive pictures received the highest valance ratings (M=6.36  .23) followed
by neutral images (M=5.37  .09) and negative images (M= 2.08  .12). There were no
other significant effects.
At the end of the study, we administered the Consortium to Establish a Registry of
Alzheimer's Disease (CERAD) word list memory test (Welsh et al., 1994) in order to
exclude possible cases of dementia from our participant group. For this test, participants
learned a list of 10 words and were later asked to recall and recognize them. In the
standard CERAD test, recall and recognition tests are given across three-time periods. In
the current study, we administered the tests once immediately after the learning phase due
to the time constraints; thus, the average scores would have been slightly lower if we had
used the standard procedures. The proportion of words recalled was computed, and
corrected recognition scores for words were calculated (hits- false alarm rates). We
excluded one older participant who scored 0.1 (3.79 SD below the older adult mean) on
the recognition test from further analyses. This participant would have scored even lower
on the standard CERAD test, which is more difficult than the modified version used in
our study. The proportion of recall and recognition for the remaining participants was as
follows (M
young_recall
=.60, Range=.30-.80; M
older_recall
=.45, Range=.20-.80;
M
young_recognition
=.92, Range=.79-1.00; M
older_recognition
=.88, Range=.60-1.00).
Results
We report partial eta squared as a measure of effect size. As in the previous
ratings analyses, the negative picture of a pie with a roach, which was rated as positive by
most older participants, was excluded from all the analyses.
15

Current emotions
An independent samples t test indicated that there was a significant difference
between younger and older adults in reported positive affect (M
young
=28.13  5.20;
M
old
=33.39  8.64), t(47) = -2.54, p<.05. Furthermore, we found a significant difference
between the two groups in reported negative affect (M
young
=14.92  5.34; M
old
=11.35 
3.21), t(47) = 2.76, p<.01. Older adults reported more intense positive emotions and less
intense negative emotions than did younger adults. In the following analyses, the
positive and negative affect scores from the emotion questionnaire (Watson et al., 1988)
were included as covariates. However, we did not find a significant effect of the emotion
questionnaire scores in any of the analyses and including them as covariates did not affect
the significant findings; hence, we will not discuss it further.
Item memory
During free recall, the experimenter noted descriptions of pictures provided by
participants. Two coders later evaluated the accuracy of the descriptions, coding
participants’ descriptions with numbers that corresponded with each of the pictures. The
inter-rater reliability was .87; the coders discussed discrepancies until mutual agreement
was reached. One point was given for each accurately described picture, and the
proportion of pictures recalled for each participant was computed.
A 2 (group: younger and older) x 2 (arousal type: arousing and neutral) x 2
(association condition: association and non-association) repeated-measure ANOVA
revealed that younger adults recalled a significantly larger proportion of the pictures than
older adults did (M
young
=.26, SE=.02; M
old
=.14, SE=.02), F(1,45)=11.85, MSE=.05, p<.05,
η
p
2
=.21 (see Table 1 for all means and standard errors). Arousing pictures were more
16

likely to be recalled (M
arousing
=.29, SE=.02; M
neutral
=.11, SE=.02), F(1,45)=79.79,
MSE=.02, p<.001, η
p
2
=.64. Moreover, there was an interaction between group and
arousal, (M
young
_
arousing
=.37, SE=.03; M
young_neutral
=.14, SE=.02; M
old
_
arousing
=.21, SE=.03;
M
old_neutral
=.07, SE=.02), F(1,45)=5.55, MSE=.02, p<.05, η
p
2
=.11. The results indicated
that, overall, participants had better recall for arousing than neutral pictures; however, the
arousal-based memory enhancement was larger in younger adults. There was no main
effect of association condition and no interaction between group and association
condition. We found no interaction between association condition and arousal type.
As reported in the methods section, we found a significant group difference in
arousal rating for the neutral pictures, suggesting that older adults rated neutral pictures
as more arousing than did younger adults. To examine the effect of this difference on
item memory, we regrouped the pictures into arousing and neutral categories based on
age group ratings. Using the average arousal rating scores by each group (M
young
=4.73,
M
old
=5.11), we categorized pictures rated higher than the group average into an arousing
group and pictures rated lower than the group average into a neutral group. This resulted
in 33 arousing and 31 neutral pictures for the younger group, and 35 arousal and 29
neutral pictures for the older group. We conducted a 2 (Group) x 2 (arousal type:
arousing and neutral) repeated-measure ANOVA. There was a main effect of group,
(M
young
=.13, SE=.01; M
old
=.06, SE=.01), F(1,45)=15.00, MSE=.006, p<.001, η
p
2
=.25.
There was also a main effect of arousal, (M
arousing
=.15, SE=.01; M
neutral
=.05, SE=.01),
F(1,45)=95.80, MSE=.002, p<.001, η
p
2
=.68. We found an interaction between group and
arousal, (M
young
_
arousing
=.19, SE=.02; M
young_neutral
=.07, SE=.01; M
old
_
arousing
=.10, SE=.02;
M
old_neutral
=.03, SE=.01), F(1,45)=4.41, MSE=.002, p<.05, η
p
2
=.09. The results remained
17

the same as those from the initial analyses using the arousal categorization according to
the IAPS’ evaluation. Participants had better recall for arousing than neutral pictures;
however, the effect was larger for younger adults.
We examined differences in item memory for positively versus negatively arousing
pictures. There was no main effect of valence but was an interaction between group and
valence, (M
young_positive
=.32, SE=.04; M
young
_
negative
=.42, SE=.04; M
old_positive
=.22, SE=.04;
M
old
_
negative
=.20, SE=.04), F(1,45)=4.69, MSE=.02, p<.05, η
p
2
=.09. Younger adults had
significantly better recall for negative than positive images, F(1, 23)=7.31, MSE=.01,
p<.05, η
p
2
=.24, whereas such a difference was not found for older adults (see Figure 1A).
This pattern is consistent with previous findings of age by valence interactions in picture
recall (e.g., Charles, Mather, & Carstensen, 2003; Mather & Knight, 2005).
Location memory (within-item memory binding)
We used a 2 (Group) x 2 (arousal type) x 2 (association conditions) repeated-
measures ANOVA to examine the proportion of the location forced-choice responses that
were correct (see Table 1 for all means and standard errors). There was a marginal main
effect of group; younger adults performed better than older adults (M
young
=0.77, SE=0.03;
M
old
=0.68, SE=0.03), F(1,45)=3.70, MSE=0.09, p<.07, η
p
2
=.08. There was no main
effect of arousal suggesting that overall, there was no difference between location
memory accuracy for arousing and neutral pictures. However, there was an interaction
between group and arousal, (M
young_arousing
=.80, SE=.03; M
young_neutral
=.74, SE=.04;
M
old_arousing
=.67, SE=.03; M
old_neutral
=.70, SE=.04), F(1,45)=4.65, MSE=0.02, p<.05,
η
p
2
=.09 (see Figure 1B). Younger adults had better location memory for the arousing
than neutral stimuli, F(1,23)=6.18, MSE=0.01, p<.05, η
p
2
=.21, replicating previous
18

findings (Mather & Nesmith, 2008), whereas older adults did not perform significantly
differently in the two conditions. There was no main effect of association condition and
no interaction between group and association condition. We found no interaction
between association condition and arousal type.
To address potential effects of group differences in arousal rating on location
memory, we conducted the following analyses using participants’ arousal ratings
described in the result section of item memory. A 2 (Group) x 2 (arousal type: arousing
and neutral) repeated-measure ANOVA found no significant effects. However, the same
analysis performed only for the younger group revealed that there was a main effect of
arousal, F(1,23)=4.58, MSE=0.01, p<.05, η
p
2
=.17, indicating that younger adults had
better location memory for arousing than neutral pictures. In contrast, there was no main
effect of arousal for the older group. Arousal enhanced younger adults’ but not older
adults’ location memory, as suggested in the initial analyses.
A 2 (Group) x 2 (valence: positively vs. negatively arousing) repeated-measure
ANOVA revealed that there was no main effect of valence and no interaction between
group and valence (M
young
_
positive
=.82, SE=.04; M
young_negative
=.78, SE=.04; M
old
_

positive
=.70, SE=.04; M
old_negative
=.63, SE=.04).
Pair memory (between-item memory binding)
Corrected pair-memory scores were calculated (hits - false alarm rates). A 2
(Group) x 2 (arousal type) x 2 (association condition) repeated-measures ANOVA
revealed a main effect of group indicating that the younger adults performed significantly
better than the older adults (Myoung=0.20, SE=0.04; Mold=0.06, SE=0.04), F(1,
45)=6.93, MSE=0.12, p<.05, η p2=.13 (see Table 1 for all means and standard errors).
19

There also was a main effect of arousal, which indicated that, overall, participants had
better memory for shape-picture pairs that involved neutral pictures than for those
involving arousing pictures (Mneutral=0.21, SE=0.04; Marousing=0.04, SE=0.04),
F(1,45)=11.22, MSE=0.12, p<.01, η p2=.20 (see Figure 1C). There was no interaction
between group and arousal. These results suggest that, unlike for picture-location
binding, for both age groups, arousal impaired picture-shape binding.
The analyses using participants’ arousal ratings showed similar findings. A 2
(Group) x 2 (arousal type) repeated-measure ANOVA indicated that there was a main
effect of arousal, (M
arousing
=0.06, SE=0.03; M
neutral
=0.23, SE=0.04), F(1,45)=17.68,
MSE=0.04, p<.01, η
p
2
=.28. There was a main effect of group (M
young
=0.20, SE=0.04;
M
old
=0.09, SE=0.04), F(1,45)=5.22, MSE=0.06, p<.05, η
p
2
=.10. As in the previous
analyses using the pre-determined arousal categories, we found no interaction between
group and arousal, suggesting that arousal impaired picture-shape binding for both
groups.
Being asked to make associations between the two stimuli improved pair memory
(M
association
=0.19, SE=0.04; M
non-association
=0.07, SE=0.03), F(1,45)=5.33, MSE=0.11,
p<.05, η
p
2
=.11. We found no interaction between group and association condition,
indicating that the effect was similar for younger and older adults. There was a marginal
interaction between association condition and arousal type, F(1,45)=3.50, MSE=.10,
p<.07, η
p
2
=.07.
A 2 (Group) x 2 (association condition) repeated-measure ANOVA conducted only
for neutral items indicated that making associations enhanced memory for shape-picture
pairs that had neutral pictures (M
association
=0.31, SE=0.05; M
non-association
=0.12, SE=0.05),
20

F(1,45)=10.57, MSE=0.09, p<.01, η
p
2
=.19 (see Figure 1D). In contrast, a 2 (Group) x 2
(association condition) repeated-measure ANOVA conducted solely for arousing items
suggested that neither younger nor older adults benefited from making associations in
terms of remembering pairs that had arousing pictures (M
association
=0.06, SE=0.05; M
non-
association
=0.03, SE=0.05), p>.69.
A 2 (Group) x 2 (valence: positively vs. negatively arousing) repeated-measure
ANOVA revealed that there was no main effect of valence on pair memory and no
interaction between group and valence.
Discussion
As expected, younger adults showed significantly better item memory than did
older adults, and both groups remembered arousing pictures better than neutral ones.
Moreover, younger adults showed significantly better item memory for negative than
positive stimuli, whereas older adults showed about the same level of item memory for
both types of stimuli. This is consistent with previous findings that attention and memory
shift away from favoring negative stimuli and towards favoring positive stimuli as people
age (for a review, see Mather & Carstensen, 2005).
The current results also replicated the previous finding that overall, older adults’
location memory or within-item memory binding was poorer than that of younger adults
(Chalfonte & Johnson, 1996; Mitchell, Johnson, Raye, Mather, & D'Esposito, 2000). Our
main question was, however, to determine whether older adults, like younger adults,
show arousal-enhanced location memory. The results indicated that location memory
was enhanced by arousal in younger adults, as previously found (Mather & Nesmith,
2008); however, this arousal-enhanced location memory was not seen in older adults.
21

The simplest explanation for this age difference may be that older adults have deficits in
within-item memory binding regardless of whether stimuli are emotionally arousing or
not, and that emotional components of items do not compensate for their binding deficits.
Another possibility is that focused attention on arousing items enhanced only item
memory but not within-item memory binding for older adults. Focused attention on
emotional objects seems to occur in both younger and older adults; however, older adults’
limited cognitive resources may only enable them to remember the gist but not the details
of arousing items whereas younger adults’ greater cognitive resources may allow them to
retain both item and feature information. In fact, our results showed that older adults
performed slightly better at remembering the location of neutral than arousing items
although they had better item memory for arousing than neutral images.
It also remains possible that older adults’ poor location memory was due to a failure
to encode the feature (location) rather than a deficit in binding. However, a meta analysis
by Old and Naveh-Benjamin (2008) found an age-related deficit in various types of
associative memory including within-item memory binding, such as memory for item-
location combinations, memory for which word was spoken by which voice, and memory
for which word appeared in which font. Although age effects were larger in some
binding type categories than others, they found pronounced age differences in each
binding type category, suggesting that memory for item-location conjunctions shows
similar age effects as other types of within-feature binding.
Consistent with our hypotheses and previous findings with younger adults,
emotional components of target items did not enhance between-item memory binding in
either group. The lack of arousal-based enhancement for between-item binding is
22

predicted by Mather’s (2007) object-based framework. Furthermore, our results
suggested that arousal not only did not enhance associative memory but impaired it.
Previous research, such as on the weapon focus effect, has shown that having an arousing
item in a scene can impair memory for other aspects of the scene. Further research is
needed to reveal whether the impaired between-item associative memory can be entirely
accounted for by poorer item memory for information shown with arousing pictures or if
there is some additional deficit specific to the link between the two items.
Across age groups, shape-picture pair memory was enhanced by making
associations, but only when the pictures were neutral. The result was consistent with
previous findings showing that making connections between two items enhanced older
adults’ pair memory (Naveh-Benjamin et al., 2007). However, our results further
indicate that strategy use will not always be as effective when items contain affective
components. This may be due to the fact that emotional components of items attract so
much attention that strategy use does not enhance memory for other irrelevant objects
presented with the items. In our experiment, participants made perceptual associations
between items; future studies should examine whether making other types of
associations, such as semantic associations, would improve memory for arousing-neutral
item pairs.
Lastly, potential methodological issues need to be considered. Although the
number of stimuli was selected with the objective of maintaining above-chance
performance in older adults and avoiding a ceiling effect in younger adults, it remains
possible that the present results were partially due to the limited number of stimuli. It
appears that we were able to avoid creating a ceiling effect in younger adults in all
23

memory tests, but there may be a possible floor effect in older adults in the pair memory
test. Another potential issue was that we could not randomize the order of memory tests,
as the nature of the tests required the tests to be conducted in a particular order (i.e., we
had to give the location test before the pair memory test, as the pair memory test would
reveal the answer to the location test.) It is possible that giving the pair memory test last
contributed to the result that arousal did not enhance between-item memory binding.
Future studies can also be improved by using the same test procedures for within-item
and between-item memory binding in order to directly compare the performance of the
two types of memory binding.
In summary, the overall findings in this study were consistent with the object-based
framework, which suggests that arousal-enhancement occurs for within-object memory
binding but not for between-object memory binding (Knight et al., 2007). Age
differences, however, were seen in the effect of arousal on within-item memory binding -
- arousal did not enhance older adults’ within-object memory binding. The parsimonious
explanation may be that older adults have binding deficits regardless of types of stimuli.
However, before drawing this conclusion, we conducted two additional experiments
using similar methods. The next two experiments also included people with Alzheimer’s
disease (AD) in order to examine the effects of emotional arousal on memory binding in
AD as compared with normal aging.
24

Table 1. Proportion of Items Recalled and Location and Pair Memory Accuracy for
Arousing (Positive and Negative) vs. Neutral Items in Association vs. Non-association
Conditions

Recall Younger Older
Arousing-positive Association .41 (.07) .29 (.07)
Non-association .24 (.04) .15 (.04)
Arousing-negative Association .45 (.05) .17 (.05)
Non-association .39 (.06) .22 (.07)
Neutral Association .17 (.03) .06 (.03)
Non-association .11 (.03) .09 (.03)
Location memory
Arousing-positive Association .84 (.05) .70 (.05)
Non-association .80 (.05) .70 (.05)
Arousing-negative Association .72 (.05) .70 (.05)
Non-association .83 (.05) .67 (.06)
Neutral Association .72 (.05) .69 (.05)
Non-association .76 (.04) .71 (.04)
Pair memory
Arousing-positive Association .08 (.11) -.02 (.11)
Non-association .10 (.07) -.11 (.08)
Arousing-negative Association .10 (.09) .07 (.10)
Non-association .21 (.10) -.09 (.10)
Neutral Association .37 (.07) .26 (.07)
Non-association .17 (.07) .07 (.07)

Note: Standard errors are in parentheses.
25

Figure 1. Proportion of Items Recalled, and Location and Pair Memory Accuracy
(A) Younger adults had better item memory for negative than positive photographs but
older adults did not show this advantage for negative pictures. Arousing pictures (B)
enhanced younger adults’ location memory, but (C) impaired both groups’ pair memory.
(D) However, strategy use (association condition) enhanced memory for shape-
photograph pairs that had neutral photographs. Error bars display the standard error.

26

1.2 The Effect of Emotional Arousal on Memory Binding in Normal Aging
and Alzheimer’s Disease
3

Kaoru Nashiro and Mara Mather

While Experiment 1 (in 1.1 of Chapter 1) focused on associative memory in
normal aging, this study (Experiments 2 & 3) will examine the effects of emotional
arousal on associative memory in normal aging and Alzheimer’s disease (AD). Given
normal age-related associative memory deficits discussed previously, it is not surprising
that people with AD face further challenges in remembering associative details. In fact,
associative learning deficits are an early sign of AD, and associative learning tasks are
used to help detect the disease (Blackwell et al., 2004; Fowler, Saling, Conway, Semple,
& Louis, 2002; Lindeboom, Schmand, Tulner, Walstra, & Jonker, 2002; O'Connell et al.,
2004). Moreover, associative learning tests can help differentiate AD from other types of
dementia, such as vascular dementia and frontotemporal lobar degeneration (Lindeboom
et al., 2002), and help predict who will develop Alzheimer’s disease (Fowler et al., 2002).
AD patients have difficulty remembering various types of associative features, including
item-location pairs commonly tested in the Paired Associative Learning Subtest of the
Cambridge Neuropsychological Test Automated Battery (Swainson et al., 2001), item–
color

pairs (Parra et al., 2009), and interactive picture pairs, such as a monkey holding

an
umbrella (Lindeboom et al., 2002).
Despite the prevalence of memory binding impairments among older and AD
individuals, little research has been conducted on whether and how this deficit can be

3
This is an already published paper with some modifications in order to fit within the
organization of the dissertation.
27

minimized. Previous studies with younger adults, however, have demonstrated that
emotional content can facilitate associative memory (Doerksen & Shimamura, 2001;
Hadley & Mackay, 2006; Kensinger & Corkin, 2003; MacKay & Ahmetzanov, 2005).
For instance, for younger adults, arousal elicited by target pictures predicts better
memory for associations between items and their intrinsic features (picture-location
combinations), a relationship that held up for both positive and negative pictures (Mather,
Gorlick, & Nesmith, 2009; Mather & Nesmith 2008; Mather & Sutherland, 2009).
Does emotional arousal enhance within-item memory binding in older adults, as
previously observed in younger adults? The previous research investigating this question
reveals a mixed picture. Kensinger, O'Brien, Swanberg, Garoff-Eaton, and Schacter
(2007) examined whether emotional content improves younger and older adults’ reality-
monitoring by having participants see or imagine neutral, positive, and negative items
during the study phase and later testing them on whether the items were seen, imagined,
or new. In Experiment 1, they found that younger adults showed enhanced memory for
the source of negative items compared with positive and neutral items, whereas older
adults did not show significant differences in reality monitoring for emotional and neutral
items. In Experiment 2, with a different “imagined” task, both age groups showed
reality-monitoring enhancement only for negative items. Similarly, another study
demonstrated that older adults performed as well as younger adults in making
associations between an item, its perceptually neutral information and its conceptually
emotional information (e.g., the Horizon by Mazda was red and was rated as dangerous),
whereas they showed impairments in making associations between an item, its
perceptually neutral information and its conceptually neutral information (e.g., the
28

Horizon by Mazda was a red luxury car; May, Rahhal, Berry, & Leighton, 2005). In
contrast, our Experiment 1 examining memory for picture locations (reported in 1.1 of
Chapter 1) found that, whereas younger adults remembered the locations of emotional
pictures better than the locations of neutral pictures, older adults did not show this
arousal-enhanced memory binding. However, given evidence that the ability to detect
emotionally arousing stimuli is relatively stable with normal aging (Knight et al., 2007;
Leclerc & Kensinger, 2008; Mather & Knight, 2006) and that the effects of emotional
arousal on memory remain similar in normal aging (Denburg, Buchanan, Tranel, &
Adolphs, 2003; Kensinger, Brierley, Medford, Growdon, & Corkin, 2002), it seems
possible that salience of emotional stimuli also facilitates older adults’ memory binding,
even if it does so less than for younger adults. Thus, one goal of the current study was to
see if we could find evidence of arousal-enhanced memory binding in older adults, and if
so, if it would be similar for positive and negative arousing stimuli or only appear for
negative stimuli as in Kensinger et al.’s (2007) study.
Does emotional arousal mitigate within-item memory-binding deficits in patients
with AD? To minimize these patients’ memory deficits, it may be possible to use their
remaining skills. Some studies suggest that the ability to process emotional information
is relatively preserved in AD patients compared with their general cognitive ability
(Bucks & Radford, 2004; Koff, Zaitchik, Montepare, & Albert, 1999) and compared with
normal controls (Lavenu, Pasquier, Lebert, Petit, & Van der Linden, 1999; Luzzi,
Piccirilli, & Provinciali, 2007; Roudier et al., 1998). Furthermore, there is some evidence
that their ability to recall emotional items is better than their ability to recall non-
emotional items (Kazui, Mori, Hashimoto, & Hirono, 2003; Moayeri, Cahill, Jin, &
29

Potkin, 2000; Satler et al., 2007). However, these findings are challenged by other
studies demonstrating that emotional content has no effect on AD patients’ memory
(Abrisqueta-Gomez, Bueno, Oliveira, & Bertolucci, 2002; Budson et al., 2006). The
discrepancy seems to come from the fact that stimuli used in these experiments vary in
intensity; prior studies demonstrating emotion-enhanced memory in AD patients used
stimuli with high emotional intensity, such as natural disasters and the 9/11 terrorist
attack, whereas those showing inconsistent results used stimuli with relatively low
emotional intensity (for a review, see Kensinger, 2006). Taken together, these results
suggest that AD patients may benefit from emotional salience of highly arousing stimuli
in order to enhance within-item memory binding.
To summarize, evidence from previous studies indicates that older adults have
memory binding deficits relative to their younger counterparts, and that associative
memory and learning are even more severely affected by AD. Previous research has also
suggested that emotional arousal enhances younger adults’ within-item memory binding,
but it is unclear whether the same effect applies to healthy older adults and patients with
AD. Since in previous studies, AD patients demonstrated emotional memory
enhancement only for materials with high intensity, we selected stimuli pre-rated high in
arousal (higher than 5 on a scale of 1 to 9, with 1 being not at all arousing and 9 being
extremely arousing). This allowed us to examine the effect of a high level of arousal on
item memory and memory binding.
30

Experiment 2
Method
Participants
We recruited 18 younger adults (M
age
=20.72 years, 3 males, 15 females, age range
18-25 years, M
education
=14.61 years), 18 older adults over 60 years old who had not been
diagnosed with dementia or other cognitive disorders from various retirement
communities (M
age
=72.67 years, 6 males, 12 females, age range 62-83 years,
M
education
=15.03 years), and 18 patients with a clinical diagnosis of probable Alzheimer's
disease from Alzheimer’s Association early stage support groups in the Lafayette,
Mountain View, Santa Cruz, and Rancho Mirage offices in California (M
age
=72.44 years,
11 males, 7 females, age range 55-86 years, M
education
=16.22 years). Neuropsychological
assessments were conducted by their respective physicians, neurologists, psychiatrists,
and neuropsychologists. The neuropsychological tests used for the diagnosis of AD
varied by clinician and included the Dementia Rating Scale (Mattis, 1988),
Neurobehavioral Cognitive Status Examination (Mueller, Kiernan, & Langston, 2001),
Wechsler Memory Scale III Logical Memory (Wechsler, 1997), and Delis-Kaplan
Executive Function Scale (Delis, Kramer, &, Kaplan, 2001). To confirm the diagnoses of
the disease, we asked participants to provide their diagnostic records.
In our experiment, we administered the Consortium To Establish A Registry Of
Alzheimer's Disease (CERAD) word list memory test (Welsh et al., 1994) to all
participants except for one healthy older adult who had time constraints. In this test,
participants learned a list of 10 words and were later asked to recall and recognize them.
In the standard CERAD, recall and recognition tests are given across three-time periods.
31

In the current study, due to the time constraints, we administered the tests once
immediately after the learning phase; thus, the average scores would have been slightly
lower if we had used the standard procedures. There were significant group differences
in the proportion of words recalled (M
young
=.57, Range=.30-.80; M
old
=.46, Range=.10-
1.00; M
AD
=.21, Range=.00 -.50), F(2,50)=18.13, MSE=.04, p<.001, and in corrected
recognition scores (hits- false alarm rates) for words (M
young
=.97, Range=.80-1.00;
M
old
=.84, Range=.40-1.00; M
AD
=.53, Range=.00-.90), F(2,50)=29.66, MSE=.03, p<.001.
Post hoc test revealed that younger and older controls preformed significantly better than
the AD group on both tests, but there were no significant differences between the
younger and healthy older groups.
Due to the different gender ratio among the three participant groups, we included
gender as a covariate in all analyses. There were no significant effects of gender in any
of the analyses; hence, we will not further discuss gender. Participants received
monetary compensation, and the experiments were conducted either in the lab, at
participants’ homes or at senior centers, using a laptop.
Materials
We used 64 photographs from the International Affective Picture System (IAPS;
Lang, Bradley, & Cuthbert, 1999) and from other sources. The photographs consisted of
matched pairs of neutral and arousing pictures that were similar in appearance,
complexity, content and focus of interest (for examples see Mather & Nesmith, 2008).
We used IAPS ratings and pre-ratings by 10 undergraduates for picture selection and
categorization (neutral, arousing-positive, and arousing-negative). We intermixed the
arousing and non-arousing photographs and made two sets of 32 photographs (Set A, Set
32

B) each of which contained an equal number of arousing and non-arousing photographs
and had only one version from any matched picture pair. For example, Set A contained a
neutral version from photograph pair 1, and therefore did not have the arousing version
from that pair. Participants were randomly assigned to view Set A or Set B. Of the 32
photographs seen by each participant, 16 were neutral, and 16 were arousing images.
Half of the arousing items were positive, and half were negative.
We also used 32 abstract shapes as stimuli, each of which was presented with a
photograph. Picture-shape pairs were displayed with our initial purpose of examining
memory for pairs as a test of between-item memory binding. However, the results
showed that AD and older groups’ pair memory performance was at floor level. Thus,
we will not discuss this further. We used PsyScope software (Cohen, MacWhinney,
Flatt, & Provost, 1993) to present the stimuli and record the participants’ responses. The
screen was divided into 3 x 3 grids, the outer eight cells of which were used to present the
images. On each slide, one picture and one shape simultaneously appeared in two of the
eight cells. One image (either a picture or a shape) was always located higher than the
other. Each stimulus type appeared in each location equally frequently.
Procedure
Encoding was incidental; participants were instructed to view the items on the
screen as if they were watching a slide show and were not informed about the upcoming
memory tests. There were six blocks, each with 16 picture-shape pairs shown one pair at
a time. Participants viewed all 32 picture-shape pairs in the assigned set across the first
two blocks, which were then repeated in the second two blocks and the third two blocks
in the same order. In order to keep the participants engaged, we asked them to do various
33

encoding tasks. In three of the six blocks, each picture-shape pair was presented in two
of the eight outer cells for 5000 ms. Immediately after the two images disappeared,
either a blue or red dot was randomly presented in one of the eight outer cells of the
screen with the question “is the dot blue or red?” in the center of the screen. The
participants were asked to indicate their answers by pressing one of the keys labeled with
a blue sticker or a red sticker. In the other three blocks, the following question appeared
in the center of the screen during stimulus presentations: “is the picture higher (H) or
lower (L) than the shape?” The participants responded by pressing one of the keys
marked “H” or “L”, at which point the next pair was presented. The two questions
alternated between blocks, and the order of which question came first was randomized
(i.e., half of the participants saw the first 16 picture-shape pairs in Blocks 1, 3, and 5 with
the blue/red question and saw the second 16 picture-shape pairs in Blocks 2, 4, 6 with the
high/low question. The other half saw the first 16 pairs in Blocks 1, 3, and 5 with the
high/low question and saw the second 16 pairs in Blocks 2, 4, 6 with the blue/red
question). The types of questions participants received during encoding had no
significant effects on their memory performance.
Immediately after the encoding phase, participants completed recall and location
memory tests. In the recall test, participants were asked to describe as many pictures as
they could remember in as much detail as possible. The location memory test assessed
within-item memory binding, or how well participants remembered combinations of
pictures and an intrinsic feature of the picture (its location). The test was a two-
alternative forced choice in which each of the 32 pictures was presented in two different
locations with number labels (one in its original location and another in a new location).
34

Participants were asked to indicate in which location they believed the picture had
appeared in during the encoding trials by pressing one of the keys marked 1 through 8. A
pair memory test was given last to examine how well participants remembered picture-
shape combinations. As mentioned earlier, these pair memory results will not be
presented here since both groups’ performance was near floor level.
Results
Item memory
During free recall, the experimenter documented participants’ descriptions of
pictures. Two coders later evaluated the accuracy of the descriptions, coding
participants’ descriptions with numbers that corresponded with each of the pictures.
Inter-rater reliability was .96; the coders discussed discrepancies until mutual agreement
was reached. One point was given for each accurately described picture, and the total
points were calculated for each participant. The proportion of pictures recalled of each
type was computed.
A 3 (group: younger, older and AD) x 2 (arousal type: arousing and non-arousing)
repeated-measures ANOVA revealed a main effect of group (M
young
=.29, SE=.02;
M
old
=.23, SE=.02; M
AD
=.06, SE=.02), F(2,51)=28.27, MSE=.02, p<.001, η
p
2
=.53.
Tukey's post hoc analysis showed that younger and older adults recalled a significantly
greater proportion of pictures than did the AD group (p<.001 for both comparisons),
whereas younger and older adults did not differ significantly (p=.22). There was a main
effect of arousal, indicating that arousing pictures were more likely to be recalled than
non-arousing pictures (M
arousing
=.29, SE=.02; M
non-arousing
=.09, SE=.01), F(51,1)=86.83,
MSE=.01, p<.001, η
p
2
=.63. We also found an interaction between group and arousal,
35

F(52,2)=14.16, MSE=.01, p<.001, η
p
2
=.36 (see Table 2 for all means and standard errors).
Separate analyses for each group indicated that all groups recalled significantly more
arousing than non-arousing pictures; however, the effect of arousal was greater in
younger adults, F(1,17)=53.02, MSE=0.01, p<.001, η
p
2
=.78, and healthy older adults,
F(1,17)=33.70, MSE=0.02, p<.001, η
p
2
=.67, than in AD patients, F(1,17)=5.64,
MSE=0.01, p<.05, η
p
2
=.25.
To examine the effect of valence, we conducted a 3 (group) x 2 (valence: positively
vs. negatively arousing) repeated-measures ANOVA. We found a main effect of valence
(M
negative
=.26, SE=.03; M
positive
=.32, SE=.02), F(1,51)=5.84, MSE=.01, p<.05, η
p
2
=.10,
indicating that participants across the groups recalled more positive than negative
pictures. There was no significant interaction between group and valence (see Table 2).
Location memory (within-item memory binding)
We used a 3 (group) x 2 (arousal type) repeated-measures ANOVA to examine the
proportion of location forced-choice responses that consisted of correct responses (Figure
2). There was a main effect of group (M
young
=.88, SE=.04; M
old
=.83, SE=.04; M
AD
=.61,
SE=.04), F(2,51)=15.17, MSE=.05, p<.001, η
p
2
=.37. Tukey's post hoc analysis showed
that younger and older adult controls performed significantly better than the AD group
(p<.001 for both comparisons), whereas younger and older adults did not differ
significantly (p=.67). There was a main effect of arousal indicating that arousal enhanced
location memory (M
arousing
=.79, SE=.02; M
non-arousing
=.76, SE=.02), F(2,51)=5.28,
MSE=.01, p<.05, η
p
2
=.09, but no interaction between group and arousal, F(2,51)=.08,
MSE=.01, p=.92, η
p
2
=.003 (see Table 2).
36

The effect of valence on location memory was analyzed with a 3 (group) x 2
(positively vs. negatively arousing) repeated-measures ANOVA. There was no main
effect of valence and no interaction between group and valence (see Table 2). The AD
group appeared to benefit more from negative than positive context but the difference
was not significant (p=.25).
Discussion
All groups recalled a greater number of arousing and non-arousing items.
However, the effect of arousal on recall was smaller in the patient group than control
groups, suggesting that the benefit of emotional content on item memory is present but
does diminish with the disease. Moreover, participants across groups demonstrated
similar memory enhancement for the locations of arousing items than the locations of
non-arousing items.
In contrast with this finding of consistent arousal-enhanced location memory
across age groups, Experiment 1 (1.1 of Chapter 1) found that healthy older adults
showed no arousal-based enhancement in within-item memory binding. The encoding
procedures in the two studies were identical except that we repeated stimuli twice in the
current experiment rather than once as in the previous study. Thus, one possible
explanation for why the current study found more evidence for arousal-enhanced memory
binding than the previous study was that, while reducing encoding load by repeating
items more frequently, repetition increased the effect of arousal on location memory for
older adults. Thus, in the second experiment we tried increasing repetition further to see
if we could replicate the current results.
37

One limitation of Experiment 2 was the unbalanced gender ratio in our sample;
we had fewer males than females in the younger and older groups. Our initial analyses
indicated that gender had no effect on item memory and memory binding. However,
given previous findings on gender differences in emotional memory at both behavioral
and neural levels (Canli, Desmond, Zhao, & Gabrieli, 2002), it is important to further
clarify that our results were not specific to any gender. In Experiment 3, we attempted to
have a more balanced gender ratio within and across groups.
Experiment 3
In the next experiment, we were interested in replicating and extending the results
from Experiment 2. As repetition seemed to increase the effect of arousal for older
adults, we increased the number of repetitions from two to three. In addition, in order to
further reduce cognitive load during encoding, we presented fewer items (16 pictures
instead of 32). With these changes, we aimed to determine 1) whether the memory
advantage for arousing stimuli observed in recall in Experiment 2 would be replicated for
recognition memory, and 2) whether the enhanced location memory for arousing pictures
would be replicated.
Method
Participants
We recruited 24 younger adults (M
age
=19.17 years, 7 males, 17 females, age range
18-21 years, M
education
=12.88 years), 24 older adults over 60 who had not been diagnosed
with dementia or other cognitive disorders from various retirement communities
(M
age
=74.89 years, 7 males, 17 females, age range 65-89 years, M
education
=13.18 years),
and 18 patients with a clinical diagnosis of probable Alzheimer's disease from
38

Alzheimer’s Association early stage support groups in the Lafayette, Mountain View, and
Santa Cruz offices in California (M
age
=73.50 years, 8 males, 10 females, age range 58-90
years, M
education
=16.83 years). Neuropsychological assessments were conducted by their
respective physicians, neurologists, psychiatrists, and neuropsychologists. To confirm
the diagnoses of the disease, we asked participants to provide their diagnostic records.
All AD participants were diagnosed with mild probable Alzheimer's disease within two
years prior to participating in this study. No patient had a history of stroke, head injury,
or other neurological illness.
The CERAD was conducted in the same manner as in Experiment 2. One healthy
older adult and one AD patient did not complete the tests due to time constraints.
Compared with the AD group, younger and older controls had significantly higher scores
on the word recall test (M
young
=.48, Range=.20-.80; M
old
=.45, Range=.20-.80; M
AD
=.16,
Range=.00 -.50), F(2,61)=25.56, MSE=.02, p<.001, and on the recognition test (hits-
false alarm rates), (M
young
=.89, Range=.70-1.00; M
old
=.86, Range=.50-1.00; M
AD
=.45,
Range=.00-.90), F(2,61)=31.28, MSE=.04, p<.001. There was no difference between the
younger and older control groups on either test.
Due to the different gender ratio and levels of education in the two participant
groups, we included gender and education as covariates in all analyses. There were no
significant effects of gender and education in any of the analyses; hence, we will not
discuss them further. Participants received monetary compensation, and the experiments
were conducted either in the lab, at participants’ homes or at senior centers, using a
laptop.
Materials
39

We used the same 64 photographs as in Experiment 2, which were divided into
Set A and Set B. Participants were randomly assigned to view either set. Half of the
assigned set was used as study materials, and the other half as lures in the recognition
test. Which half of the set was presented during the study phase was randomized, and
each set contained an equal number of neutral and arousing photographs. In order to
keep the procedure consistent with that in Experiment 2, we presented the 32 shapes used
in Experiment 2 together with the photographs.
Procedure
The procedure was the same as that in Experiment 2 except for the following
modifications. There were four blocks of trials; in each of these participants viewed the
same set of 16 photograph-shape pairs one at a time. Various encoding tasks were given
to the participants to keep them engaged. The encoding task in Block 1 and 4 were the
same as the dot color identification task used in Experiment 2 (participants indicated
whether the dot was blue or red between trials). The task in Block 2 was identical to the
other encoding task described in Experiment 2 in which participants indicated whether
the photograph was higher or lower than the shape. In Block 3, participants were asked:
“is the photograph bigger (B) or smaller (S) than the shape?” Participants answered by
pressing one of the keys marked “B” or “S”, at which point the next pair was presented.
Immediately after the encoding phase, participants completed recognition and
location memory tests. In the recognition test, we randomly presented 16 studied and 16
non-studied photographs and asked participants to indicate whether they had seen the
pictures in the study session by pressing one of the keys marked “YES” or “NO”. The
location memory test was the same as that in Experiment 2. A pair memory test was
40

given last, but the results will not be discussed here, as again, performance was near floor
on this test.
Results
Item memory
Corrected recognition scores were calculated (hits - false alarm rates). A 3 (group:
younger, older and AD) x 2 (arousal type: arousing and non-arousing) repeated-measures
ANOVA revealed a main effect of group (M
young
=0.85, SE=0.04; M
old
=0.74, SE=0.04;
M
AD
=0.53, SE=.05), F(2,63)=12.91, MSE=0.08, p<.001, η
p
2
=.29. Tukey's post hoc
analysis showed that younger and older adults recognized a significantly greater
proportion of pictures than did the AD group (p<.001 and p=.004, respectively), whereas
younger and older adults did not differ significantly (p=.18). There was a main effect of
arousal (M
arousing
=0.73, SE=0.03; M
non-arousing
=0.68, SE=0.03), F(2,63)=4.21, MSE=0.02,
p<.05, η
p
2
=.06, but no interaction between group and arousal (p=.28). A 3 (Group) x 2
(valence: positively vs. negatively arousing) repeated-measures ANOVA revealed that
there was no main effect of valence but a significant interaction between group and
valence, F(2,63)=3.60, MSE=.03, p<.05, η
p
2
=.10 (see Table 2). Further analyses
suggested that the AD group had better recognition memory for negative than positive
pictures, F(1,17)=4.21, MSE=.04, p=.06, η
p
2
=.20, although the difference was only
marginally significant. Neither younger nor older healthy controls showed a significant
difference between memory for negative and positive pictures.
In addition, the hit and false alarm rates were separately examined. A 3 (group:
younger, older and AD) x 2 (arousal type: arousing and non-arousing) repeated-measures
ANOVA of hit rates revealed no significant findings. The same analysis for false alarm
41

rates found a main effect of group, F(2,63)=19.42, MSE=.03, p<.001, η
p
2
=.38 (see Table
3 for all means and standard errors). Tukey's post hoc analysis suggested that AD
patients made more false alarms than did the younger and older groups (p<.001 for both
comparisons), whereas younger and older adults did not differ significantly (p=.507). A
3 (Group) x 2 (valence: positively vs. negatively arousing) repeated-measures ANOVA
of hit rates revealed a main effect of group, F(2,63)=3.41, MSE=.06, p<.05, η
p
2
=.10,
suggesting that younger adults obtained significantly more hits than did AD patients. The
same analysis for false alarm rates found a main effect of group, F(2,63)=14.58,
MSE=.04, p<.001, η
p
2
=.32, suggesting that AD patients made significantly more false
alarms than did the two other groups. Overall, we did not find the effects of emotion and
valence on false alarm rates in any groups (Gallo, Foster, Wong, & Bennett, 2010,
Kapucu, Rotello, Ready, & Seidl, 2008; Thomas & Hasher, 2006). However, this lack of
effects of valence on false alarms may have been due to very low false alarm rates in the
younger and older groups.
Location memory
Location memory accuracy was calculated by the proportion of correct responses of
the total responses. A 3 (group) x 2 (arousal type) repeated-measure ANOVA revealed a
main effect of group (M
young
=0.86, SE=0.03, M
old
=0.76, SE=0.03, M
AD
=0.62, SE=0.04), F
(2,63)=15.11, MSE=0.04, p<.001, η
p
2
=.32. Tukey's post hoc analysis showed that
younger and older adults performed significantly better than the AD group (p<.001 and
p=.005, respectively), whereas younger and older adults did not quite differ significantly
(p=.05). There was a main effect of arousal (M
arousing
=0.77, SE=0.02; M
non-arousing
=0.72,
SE=0.02), F (2,63)=5.60, MSE=0.02, p<.05, η
p
2
=.08, but no significant interaction
42

between group and arousal. The results were consistent with those in Experiment 2,
indicating an overall arousal-based enchantment of location memory that did not
significantly differ between the groups.
The effect of valence on location memory was analyzed with a 3 (group) x 2
(positively vs. negatively arousing) repeated-measures ANOVA. There was no main
effect of valence and no interaction between group and valence (see Table 2).
Discussion
Arousal enhanced item memory for healthy younger and older adults, but the
effect was diminished for AD patients. The results of location memory were also similar
to those in Experiment 2. We found a main effect of arousal but no group by arousal
interaction; suggesting that, in general, participants had better memory for the locations
of arousing than non-arousing pictures. Valence had little influence on location memory
in all groups.
General Discussion
Experiments 2 and 3 examined the effect of arousal on item memory and within-
item memory binding in healthy younger and older adults and AD patients. However,
our previous study using similar methods (Experiment 1) revealed that, whereas younger
adults showed arousal-enhanced location memory, older adults did not. Given mixed
findings in previous research, the current study further probed the effects of arousal on
older adults’ location memory to see if there are any benefits of emotional arousal for
location memory binding when using easier memory tasks than in Experiment 1.
The results from Experiments 2 and 3 revealed that healthy older adults and AD
patients remembered a greater number of arousing than non-arousing items, indicating
43

that emotional arousal enhances item memory in normal aging and in AD, although the
item memory enhancement effect was smaller in the patient group. Importantly,
participants across groups had better memory for the locations of arousing than non-
arousing pictures, whereas valence had little influence on location memory. The results
demonstrate that the effects of emotional salience on within-item memory binding
previously found in younger adults (Mather et al., 2009; Mather & Nesmith 2008; Mather
& Sutherland, 2009) are similarly present in older adults with and without AD.
Task difficulty may play a role in determining the size of the arousal effect for
older adults with and without AD. In Experiment 1, healthy older participants viewed 32
pictures twice and showed no arousal enhancement in location memory. In Experiment
2, we presented the same number of items three times, and older participants showed
better location memory for arousing than non-arousing pictures. In Experiment 3, we
reduced encoding load further by increasing the number of presentations to four and
reducing the number of pictures to 16. In Experiment 2 and 3, older adults showed an
effect of arousal on location memory, with a larger effect in Experiment 3 (Ms = .85 vs.
.81 for arousing vs. non-arousing in Exp. 2 and Ms = .82 vs. .70 in Exp. 3). One possible
interpretation of these results is that combining the benefits of emotional salience and
adequate exposure to items in the present study led to location memory enhancement in
healthy older adults. Since older adults have age-related memory binding deficits to
begin with, they may need more exposure to stimuli than younger adults to benefit from
arousing content to enhance within-item feature binding. In the case of AD patients, it is
unclear whether more exposure to items would benefit them since they showed similar
44

effects of arousal on location memory in Experiments 2 and 3 (Ms = .63 vs. .59 for
arousing vs. non-arousing in Exp. 2 and Ms = .64 vs. .59 in Exp. 3).
Why would arousal enhance within-item memory binding? The arousal-biased
competition theory (Mather & Sutherland, 2011) proposes that an emotional item has
high priority and captures attention when there is no other competing high priority
information. This arousal-induced attention enhances within-item feature binding,
leading to deeper encoding and thus better retention of bound information (see Mather &
Sutherland, 2011, for further discussion of this issue). Previous research has shown that
the ability to detect emotionally arousing stimuli is relatively stable with normal aging
(Knight et al., 2007; Leclerc & Kensinger, 2008; Mather & Knight, 2006). Prior
evidence also suggests that AD patients have normal physiological responses to
emotional stimuli (Hoefer et al., 2008) and the ability to process emotional information as
well as do healthy controls (Lavenu et al., 1999; Luzzi et al. 2007; Roudier et al., 1998).
Furthermore, the effects of emotional arousal on memory remain similar in normal aging
(Denburg et al., 2003; Kensinger et al., 2002) and are relatively well preserved in AD
(Kazui, Mori, Hashimoto, & Hirono, 2003; Moayeri, Cahill, Jin, & Potkin, 2000; Satler et
al. 2007). Preserved arousal enhancement of memory in both groups seem to compensate
for their memory binding impairment when memory tasks are relatively easy, as
evidenced by our finding that participants across groups had better location memory for
arousing than non-arousing pictures. Presumably, arousing components of items
attracted their attention, which strengthened perceptual binding and hence enhanced
memory for within-item features.
45

Our results were in line with previous studies suggesting that emotional
information embedded in target items enhanced older adults’ source memory (May,
Rahhal, Berry, & Leighton, 2005; Rahhal, May, & Hasher, 2002). However, there is also
counter-evidence suggesting that neither younger nor older adults showed benefits of
emotional content on source memory (Davidson, McFarland, & Glisky, 2006). One
possible explanation for this discrepancy is differences in levels of task difficulty across
studies. As described earlier, our previous and current results together suggest that
healthy older adults benefit more from emotional content when tasks are relatively easy.
Thus, it is possible that studies suggesting no effect of emotion on source memory used
tasks that are cognitively challenging for older adults. However, the fact that Davidson et
al. (2006) failed to replicate previous findings on beneficial effects of emotion on source
memory by using similar methods as those in previous studies (Doerksen & Shimamura,
2001; Kensinger & Corkin, 2003) warrants further investigation into discrepancies across
studies.
One limitation of the current study was younger adults’ possible ceiling effects in
location memory, indicating that the tasks were too easy for them, which may have
reduced any potential arousal effects. Future studies should use more appropriate levels
of task difficulty for each group to avoid this issue. Another limitation of the current
study was the small number of stimuli. Although the low number of stimuli was
intentionally selected, it might have been limited our ability to observe larger effects of
emotion on memory performance. Despite these limitations, the current study provides
important information about the benefits of emotional arousal on older adults’ and AD
46

patients’ memory binding. These findings may lead to strategies to help reduce memory-
binding impairments previously observed in both groups.

47

Table 2. Item and Location Memory Accuracy for Neutral, Negative and Positive Items.
For Experiment 2, proportion of total items of that type that were recalled is reported; for
Experiment 3, corrected recognition (hits – false alarms) is reported. Location memory is
the proportion of responses that were correct.

Experiment 2
Recall Younger Older AD
Arousing .42 (.04) .38 (.04) .08 (.04)
negative .41 (.04) .33 (.04) .06 (.04)
positive .43 (.04) .42 (.04) .10 (.04)
Non-arousing .15 (.02) .09 (.02) .04 (.02)

Location Younger Older AD
Arousing .89 (.04) .85 (.04) .63 (.04)
negative .89 (.04) .89 (.04) .66 (.04)
positive .90 (.05) .84 (.05) .59 (.05)
Non-arousing .86 (.04) .81 (.04) .59 (.04)

Experiment 3
Recognition Younger Older AD
Arousing .88 (.05) .79 (.05) .53 (.05)
negative .84 (.05) .78 (.05) .60 (.06)
positive .92 (.05) .79 (.05) .46 (.06)
Non-arousing .81 (.05) .70 (.05) .54 (.05)

Location Younger Older AD
Arousing .86 (.03) .82 (.03) .64 (.04)
negative .85 (.05) .81 (.05) .68 (.05)
positive .87 (.04) .83 (.04) .60 (.05)
Non-arousing .87 (.04) .70 (.04) .59 (.04)

Note: Standard errors are in parentheses.
48

Table 3. Item Hit and False Alarm (FA) Rates for Arousing (Negative and Positive) and
Non-arousing Items in Experiment 3.
Hits Younger Older AD
Arousing .89 (.03) .82 (.03) .75 (.04)
negative .85 (.04) .82 (.04) .78 (.05)
positive .92 (.04) .82 (.04) .72 (.05)
Non-arousing .82 (.04) .76 (.04) .78 (.05)

FAs Younger Older AD
Arousing .01 (.03) .04 (.03) .22 (.03)
negative .01 (.03) .04 (.03) .18 (.04)
positive .00 (.03) .03 (.03) .26 (.04)
Non-arousing .01 (.03) .06 (.03) .24 (.03)

Note: Standard errors are in parentheses.
49

Figure 2. Location Memory Accuracy for Arousing and Non-arousing Items
(A) In Experiment 2, healthy older adults showed better location memory for arousing
than non-arousing pictures, but the AD group did not show this advantage. (B)
Experiment 3 replicated the finding of Experiment 1.
0
0.2
0.4
0.6
0.8
1
Younger Older AD
Location Memory
Proportion of Correct Responses
Arousing
Non-arousing
B
0
0.2
0.4
0.6
0.8
1
Younger Older AD
Location Memory
Proportion of Correct Responses
Arousing
Non-arousing
A
50

CHAPTER 2: BOTH YOUNGER AND OLDER ADULTS HAVE DIFFICULTY
UPDATING EMOTIONAL MEMORIES
4

Kaoru Nashiro, Michiko Sakaki, Derek Huffman and Mara Mather

Despite clear evidence suggesting age-related deficits in associative memory,
Chapter 1 demonstrated that emotional arousal can enhance associative memory in older
adults. While this beneficial effect of emotion was found for making novel associations,
in real life, we often encounter the same people, places, or events in different contexts,
requiring us to make new associations to old information. Thus, it is important to
investigate whether emotion has the same enhancing effect for previously-learned items
(as opposed to new items examined in Chapter 1). Intriguingly, recent research with
younger adults suggests that emotion has different effects on initial versus subsequent
learning; whereas people have better associative memory for the intrinsic features of
emotional items (Mather, 2007; Mather & Sutherland, 2011), they have worse associative
memory for emotional items or precursors of emotional items that have been learned
before (Mather & Knight, 2008; Novak & Mather, 2009). One hypothesis is that initial
associative memory involving emotion is robust and resistant to extinction; therefore,
previous learning experience of emotional items interferes with new learning involving
the same emotional information. From neuroimaging perspectives (though this is not
directly tested here), our prediction is that the amygdala facilitates emotional memories
for new items, which become robust and difficult to extinguish. Therefore, the amygdala
in turn opposes updating of old emotional associations (Sakaki, Niki, & Mather, 2011).

4
This is an already published paper with some modifications in the introduction and discussion
sections in order to fit within the organization of the dissertation.
51

However, since the above studies were all conducted with younger subjects, it is
unclear whether the emotion impairing effects are also seen in older adults. Thus, the
main purpose of the current study was to test whether emotion would also impair memory
updating in older adults. Based on the associative memory deficits observed in past
studies (Naveh-Benjamin, 2000), we predicted a main effect of age group, such that
overall, older adults would have poorer associative memory than younger adults,
irrespective of an item’s emotionality or novelty. Given relatively good structural and
functional preservation of the amygdala in normal aging (for a review see Nashiro,
Sakaki & Mather, 2012), the amygdala should still facilitate learning new emotional
associations and prevent updating of old emotional associations in older adults. Thus, we
hypothesized that, like younger adults, older adults would show more difficulty learning
associations to old emotional items than to new emotional items.
Method
Participants
Thirty-two younger adults (M
age
=20.78, age range 18-29, 7 male, 25 females,
M
education
=14.71) and 32 older adults (M
age
=74.00, age range 65-93, 15 males, 17 females,
M
education
=15.97) participated. There were no significant effects of participant sex in any
of the analyses. We recruited older adults from local communities and retirement homes
who had not been diagnosed with dementia or other cognitive disorders.
Materials
The stimuli were 64 matched-pair pictures (e.g., Novak & Mather, 2009), for
which each negative picture was yoked with a visually similar but less arousing neutral
picture. Participants saw either the negative or neutral version from a pair; which version
52

was shown was counterbalanced. For each participant, 16 negative arousing and 16
neutral pictures were used as new pictures without prior associations, while the other 16
negative arousing and 16 neutral pictures were used as old pictures (the old/new sets were
counterbalanced across participants). Each old picture was randomly paired with a
drawing of a neutral object (e.g., apple).
Procedure
The experiment consisted of two parts: Part 1 was a picture-object association
phase and Part 2 was a picture-location association phase.
In Part 1, participants first studied 32 picture–object pairs. During the learning
session, participants saw a picture at the center of the screen (a location not used in the
study phase in Part 2). After 3 seconds, an object appeared in one of the bottom two
corners for 2 seconds while the picture remained on the screen. Participants were asked
to remember the pair while indicating whether the object appeared on the right or left
bottom corner by pressing a key.
The pair memory test was a 2-alternative forced choice design in which participants
saw a picture in the center of the screen and two previously seen objects in the top two
corners. They were asked to choose the object associated with the picture by pressing a
key. Since the main purpose of the current study was to examine how initial learning
affects later learning, the task was made easy to promote initial learning. To facilitate
learning, the study-test cycle was repeated once, and feedback was provided by the
correct object remaining on the screen for one second after each response.
In Part 2, participants viewed the 64 pictures (half seen in Part 1) in a randomized
order, each for 2 seconds at one of the six locations (the top three and bottom three cells
53

of a 3 x 3 grid partitioning the screen). Participants were instructed to remember picture-
location combinations while indicating whether the picture appeared higher or lower than
the center of the screen by pressing a key. In the subsequent memory test, each of the 64
pictures was presented at the center of the screen. Participants indicated each picture’s
previous location by pressing a key.
At the end of the experiment, participants provided arousal ratings for the pictures
using a 9-point scale (1= not at all arousing to 9= extremely arousing) and valence ratings
using a 9-point scale (1= extremely negative to 9= extremely positive).
Results
Picture ratings
Older adults rated two negative arousing pictures as very low in arousal (M <
3.5); thus, those pictures were excluded from all the analyses for the older group. Both
groups rated the rest of the pictures in the expected direction on arousal (M
negative
= 6.31,
SE = .17; M
neutral
= 2.56, SE = .15), F(1, 62) = 538.94, MSE = 0.83, p < .001, η
p
2
= .90,
and on valence (M
negative
= 2.58, SE = .10; M
neutral
= 5.56, SE = .11), F(1, 62) = 308.95,
MSE = 0.92, p < .001, η
p
2
= .83. In both ratings, there were no interactions between
group and valence category.
Picture-object association memory
A 2 (group: younger, older) x 2 (emotion: neutral, negative arousing) x 2 (test
cycle: Test 1, Test 2) mixed analysis of variance (ANOVA) was performed on the correct
response rates in the Part 1 memory tests. The ANOVA revealed that younger adults (M
= .97, SE = .02) performed significantly better than older adults (M

= .87, SE = .02), F(1,
62) = 19.12, MSE = 0.03, p < .001, η
p
2
= .24, and that Test 2 (M

= .96, SE = .01) yielded
54

better performance than Test 1 (M

= .89, SE = .02), F(1,62) = 42.04, MSE = 0.01, p <
.001, η
p
2
= .40. In addition, there was an interaction between group and test cycle, F (1,
62) = 11.68, MSE = 0.01, p = .001, η
p
2
= .16, suggesting that older adults (M
test1
= .82, SE
= .02; M
test2
= .92, SE = .01) showed a greater improvement in Test 2 than did younger
adults (M
test1
= .96, SE = .02; M
test2
= .99, SE = .01). As a result, both groups learned most
pairs by the second test. This initial learning was intentionally made easy (as discussed
above), which resulted in ceiling effects which may have obscured potential differences
in pair memory for neutral and negative arousing items.
Picture-location association memory
Since the purpose of the study was to examine the effects of initial learning on
subsequent memory performance, we excluded items for which participants did not show
correct memory performance by Test 2 in the initial learning phase (Part 1). A 2 (group)
x 2 (emotion) x 2 (novelty: new, old) mixed ANOVA was performed on the proportion of
correct location memory responses in Part 2. There was a significant effect of group
(M
younger
= .68, SE = .03; M
older
= .49, SE = .03), F(1, 62) = 25.21, MSE =0.09, p <.001, η
p
2
= .29. In addition, the ANOVA revealed a significant interaction between emotion and
novelty, F(1,62) = 16.13, MSE = 0.01, p < .001, η
p
2
= .21 (see Figure 3). There was no
significant interaction between group, emotion type and novelty (p = .99), indicating the
age-independent nature of the interaction. Separate 2 (emotion) x 2 (novelty) ANOVAs
for each age group also confirmed a significant interaction between emotion and novelty
for both younger adults, F (1, 31) = 9.86, MSE = 0.01, p = .004, η
p
2
= .24, and older
adults, F (1, 31) = 6.80, MSE = 0.02, p = .014, η
p
2
= .18. When pictures were negative,
location memory was worse for old than new pictures in younger adults, t(31) = 3.49, p =
55

.001, and in older adults, t(31) = 2.40, p = .023. In contrast, location memory did not
differ between old neutral and new neutral pictures in younger adults, t(31) = 0.37, p =
.714, or in older adults, t(31) = 1.01, p = .320.
Discussion
Consistent with previous findings on age-related declines in associative memory
(e.g., Naveh-Benjamin, 2000), older adults learned picture locations less well than did
younger adults. However, older and younger adults showed similar interactions of
picture novelty and emotion. For negative pictures, participants remembered more
locations of novel pictures than locations of old pictures. In contrast, for neutral pictures,
location memory did not significantly differ for old and new pictures. Importantly,
younger and older adults showed a similar pattern of interactions, indicating that the
effects of emotion on associative memory updating remain stable with age. This is
consistent with previous findings that the amygdala is relatively well preserved in aging
structurally (e.g., Allen et al., 2005) and functionally (Wright et al., 2008). Thus,
emotion seems to continue to modulate memory updating in normal aging.
Conceptually, why does emotional arousal enhance associative memory for new
items but impair it for old items? As previously discussed, arousal-biased competition
theory (Mather & Southerland, 2011) postulates that emotional arousal enhances
associative memory when there is no other competing high-priority information. Thus,
when items are new, an emotional target captures attention and increases associative
feature binding, leading to deeper encoding and better associative memory. In contrast,
when items are old, it is possible that both old and new memories with the same
emotional information have high priority and therefore compete for attention or resources.
56

Consequently, emotional arousal exacerbates the competition and impairs associative
memory for new items. Our current results suggest that these ideas apply to both younger
and older adults.
Some limitations of the study need to be mentioned. Since this is a cross-
sectional study, we cannot make strong conclusions about developmental changes or
stability in the effects of emotion on associative memory. Another limitation is that we
did not use positive arousing pictures and thus cannot address whether the observed
effects of emotion on location memory is due to arousal or valance of the stimuli. Given
older adults’ preference for positive information relative to negative information in
attention and memory (compared with younger adults; Mather & Carstensen, 2005), it is
possible that positive arousing items differentially affect younger and older adults.
Future research should also use a larger sample size to investigate potential age
differences in the magnitude of the observed emotion effects on subsequent memory.
Despite these limitations, the current study provides evidence suggesting that
emotion interacts with associative memory similarly across the two age groups. Given
age-related declines in associative memory, this line of research is important for
understanding how emotional arousal affects older adults’ memory performance. Future
research may help us further identify the costs and benefits of emotion on associative
learning and develop strategies for improving associative memory.
57

Figure 3. Picture-Location Association Memory
Younger and older adults showed similar interactions between emotion (neutral vs.
negative) and novelty (new vs. old). Both groups had worse location memory for old
negative than new negative pictures, whereas no significant differences were observed
between old neutral and new neutral items. Means are shown inside the bars. Error bars
represent standard errors. Chance performance is 1/6 (0.17).

58

CHAPTER 3: AGE-REALTED SIMILARITIES AND DIFFERENCES IN BRAIN
ACTIVITY DURING EMOTIONAL VS. NON-EMOTIONAL MEMORY UPDATING
5

Kaoru Nashiro, Michiko Sakaki, Lin Nga, and Mara Mather

The ability to update associative memory is an important aspect of episodic
memory as well as a critical skill for social adaptation, as it allows one to flexibly update
information and respond appropriately to a given situation. For example, you may place
your car keys at different places throughout the day, requiring you to update your
memory of where they are at any given point (i.e., updating key-location associations).
Also, you may see your officemate everyday but notice that he is in a bad mood on a
particular day based on the changes in his facial expression (i.e., updating person-
expression associations). Previous research found that emotional arousal alters neural
mechanisms underlying memory updating such that certain brain regions show greater
activity when updating emotional information than when updating neutral information
(Sakaki et al., 2011). However, since these studies were conducted with younger adults,
it remains unknown whether similar neural mechanisms can be seen in older adults.
Given the fact that the ability to update associative information declines with age (Mell et
al., 2005; Weiler, Bellebaum, & Daum, 2008), it is important to understand how
emotional arousal may change neural mechanisms underlying memory updating in older
adults.
Previous studies with younger adults have demonstrated that the
frontopolar/orbitofrontal (OFC) regions play a critical role in updating emotional memory.

5
The paper is in preparation for publication. This is a version with minor modifications in the
introduction and discussion sections in order to fit within the organization of the dissertation.
59

One recent study using a long-term memory paradigm (Sakaki et al., 2011) found that the
frontopolar OFC regions showed greater activity while learning new associations for old
emotional items than for new emotional items. In addition, they found that the frontal
pole had negative correlations with the amygdala when people learned new associations
to old emotional items. Consistent with these findings, our recent study using a working
memory updating task (Nashiro, Sakaki, Nga, & Mather, in press) revealed that the
frontopolar OFC regions showed greater activity while people were engaged in emotional
than neutral memory updating. The study also found greater negative correlations
between the OFC and the amygdala when updating negative associations than when
updating neutral associations. These results suggest that the frontopolar OFC helps
update old emotional memories by suppressing amygdala’s protection of old
representations. This is consistent with previous findings on the role of the amygdala in
emotional memory – it facilitates emotional memories during initial learning (LaBar &
Cabeza, 2006), which in turn can oppose updating of original representations. Taken
together, the interactions between the amygdala and the frontopolar/orbitofrontal (OFC)
region are critical for emotional memory updating.
Further evidence for a critical role of amygdala-fontopolar OFC interactions was
provided in animal experiments using reversal learning tasks in which subjects had to
update stimulus-reward contingencies based on feedback. One study (Stalnaker, Franz,
Singh, & Schoenbaum, 2007) using a reversal learning task of odor-solution associations
demonstrated that reversal learning was impaired in the OFC lesioned group but was not
affected in the amygdala lesioned group. Strikingly, damage to both OFC and amygdala
did not impair reversal learning compared to a control group without any lesions. The
60

results suggest that the amygdala protects old emotional representations making it hard to
update them, whereas the OFC opposes this amygdala effect. Extinction tasks also
require updating of associations and amygdala lesions have been shown to facilitate the
extinction of emotional instrumental responses in macaque monkeys, whereas OFC
lesions impair extinction (Izquierdo & Murray, 2005).
Since the studies described previously were all conducted with younger humans
or on animals, it remains unclear whether these neural mechanisms would also apply to
older adults. In general, evidence suggests that the amygdala remains relatively intact in
older adults (Nashiro, Sakaki, & Mather, 2012); however, previous findings on age-
related changes in the frontopolar OFC are more ambiguous. In terms of age-related
structural changes, previous research found age-related volume declines in the lateral and
orbital frontal gray matter (Tisserand et al., 2002) and in the frontal pole gray matter
(John et al., 2009; Salat, Kaye, & Janowsky, 2001). In contrast, another study (Salat et
al., 2001) found that OFC volume was a larger proportion of prefrontal volume for older
adults than for younger adults, suggesting the OFC declines less with age than other
regions. A study with a particularly large sample of participants (Pfister et al.) is
consistent with this lack of OFC decline, as negative correlations between age and
cortical thickness were seen in lateral and superior prefrontal regions, but not in the
medial OFC (Fjell et al., 2009). A functional MRI study (Lamar, Yousem, & Resnick,
2004) examined age differences in OFC function by employing delayed match and non-
match to sample tasks previously shown to elicit OFC involvement. They found that
younger compared with older adults showed greater activity in the lateral OFC (BA 47),
indicating that age-related alteration in lateral OFC recruitment contribute to older adults’
61

poor performance on the tasks. However, since this study used neutral stimuli, it is
unclear whether the same task involving emotional stimuli would also result in age
differences in lateral OFC activity. Although not emphasized in their report, the same
study also suggested that there were no age-related differences in frontopolar (BA 10)
activity during non-match in contrast to match to sample tasks, leaving the possibility that
the frontal pole functions similarly between younger and older adults.
Despite the fact that it remains unclear how age might affect the structure and
function of the frontopolar OFC regions, previous behavioral studies suggested that
younger and older adults showed similar enhancing and impairing effects of emotional
arousal on associative memory and memory updating (Nashiro & Mather, 2011a; Nashiro
Sakaki, Huffman, & Mather, in press). Thus, it seems possible that the neural
mechanisms underlying emotional memory updating might also be similar between the
two age groups. The current study used event-related functional magnetic resonance
imaging (fMRI) to examine this possibility.
Methods
Participants
Nineteen undergraduates (M
age
= 25.38, 11 males, 8 females, age range 19-35) and
22 older adults (M
age
= 68.00, 11 males, 11 females, age range 61-78) participated in the
study. The data from the younger participants are described in Nashiro et al. (in press).
Participants provided written informed consent approved by the University of Southern
California (USC) Institutional Review Board and were paid for their participation.
Prospective participants were screened and excluded for any medical, neurological, or
psychiatric illness. Two younger and two older adults were excluded from all analyses
62

due to very poor task performance (their number of errors or number of no responses was
greater than 3 standard deviations above the mean). One older adult was excluded due to
a previous stroke, which was unknown to the participant prior to the study.
Materials
The face stimuli were color images obtained from the FACES database developed
at the Max Planck Institute for Human Development (Ebner, Riediger, & Lindenberger,
2010), which included young, middle-aged and older adults’ female and male faces.
Thirty individuals’ faces, which had neutral, happy, angry, and eyeglasses
versions, were used in the main experiment. These faces were grouped into fifteen pairs
of two faces from the same age group (i.e., five pairs of younger faces, five pairs of
middle-aged faces, and five pairs of older faces), and the gender of each pair was always
the same (i.e., male-male, female-female pairs). One out of five pairs in each age
category was randomly selected and assigned to each participant, resulting in three pairs
from different age groups being used for each participant. Which of the three pairs were
used for which of the three conditions was randomly determined for each participant.
Gender of face pairs were counterbalanced across participants, such that half of the
participants saw two female pairs and one male pair while the other half saw one female
pair and two male pairs. Each of the faces in a pair randomly appeared on the left or right
side of the screen on each trial.
Behavioral Procedures
We used a reversal learning task, which is designed to test the ability to update
associative information in working memory. Before the main experiment began,
participants completed two shorter practice blocks outside the scanner. The procedure in
63

the practice session was the same as the main task described below, except that it was
shorter and had a different categorization rule. During practice, participants were asked
to identify the person who had a baseball cap and then who was sad. We used two pairs
of faces that were not used in the main experiment.
The main experiment consisted of positive, negative and neutral blocks, the order
of which was randomized across the participants. At the beginning of each block, a
prompt appeared; “Who is happy?” “Who is angry?” or “Who wears glasses?” in the
positive, negative or neutral conditions respectively. Each trial lasted for 6 seconds and
began with the presentation of two neutral faces with a white background (see Figure 4).
Participants were asked to select one face with the target characteristics (happy, angry, or
eyeglasses) by pressing a key corresponding to the left or right side of the screen.
Immediately after their response, feedback was presented for 1 second on a gray
background. If the response was correct, the selected face changed (into a happy face,
angry face, or face with eyeglasses), while the other face remained neutral. If the
response was incorrect, both of the faces remained neutral. When the participant did not
respond within 4 seconds, the warning “please respond faster” was displayed in the center
of the screen in replacement of feedback faces. The trial ended with a fixation cross for
the remainder of the 6 seconds. After three to six consecutive correct responses, the
correct face was reversed. Participants were asked to keep track of the correct face and
change their answers as soon as they noticed the switch.
Trial Modeling
Each trial was categorized as one of three trial types: reversal, acquisition and
other. ‘Reversal’ described individual trials where the participant selected the previously
64

correct person, but this led to a neutral face expression of the selected person indicating
that the correct person was just switched. Reversal trials were defined so that they were
always followed by a response shift in the next trial; thus, trials where the participant
selected the previously correct person, but did not change their response in a subsequent
trial were not included. This categorization allowed us to capture brain activity when the
participant made a final error immediately before switching their response. It should be
noted that there were no differences in terms of the perceptual properties or the stimulus
emotionality across positive, negative and neutral conditions during the reversal trials
since participants viewed two neutral faces during reversal in all conditions.
‘Acquisition’ included series of trials where the participant’s correct choices of a
particular person led to a change in the face (i.e., happy face, angry face, or face
appearing with eyeglasses). The first trial of each condition was modeled as ‘other’
(regardless of whether the subject made a correct or incorrect choice), as these trials
required subjects to guess and do not reflect learning (or failure of learning) of previous
associations. The rest of the trials, which did not fall into the categories of reversal or
acquisition trials, were also aggregated as ‘other.’ For example, ‘other’ includes trials
where the participant chose incorrect faces before reaching the criterion (three to six
consecutive correct responses) or trials where the participant failed to respond within 4
seconds.
Functional MRI Data Acquisition and Preprocessing
Imaging was conducted with a 3 T Siemens MAGNETOM Trio scanner with a
12-channel matrix head coil at the University of Southern California Dana and David
Dornsife Neuroimaging Center. The imaging parameters were repetition time (TR) =
65

2000 ms, echo time (TE) = 25 ms, slice thickness = 3 mm, interslice gap = 0 mm, flip
angle (FA) = 90°, and field of view (FOV) = 192 mm x 192 mm. Data preprocessing
were performed using FMRIB's Software Library (FSL; www.fmrib.ox.ac.uk/fsl), which
included motion correction with MCFLIRT, spatial smoothing with a Gaussian kernel of
full-width half-maximum 5 mm, high-pass temporal filtering equivalent to 100 seconds,
and skull stripping of structural images with BET. MELODIC ICA (Beckmann & Smith,
2004) was used to remove noise components. Registration was performed with FLIRT;
each functional image was registered to both the participant’s high-resolution brain-
extracted structural image and the standard Montreal Neurological Institute (MNI) 2-mm
brain.
FMRI Data Analyses.
Whole-brain analysis. For each reversal trial for each participant, stimulus-
dependent changes in BOLD signal were modeled with regressors for feedback and
fixation periods. Signal from the feedback and fixation periods were averaged for each
valence condition. The selection period (the initial presentation of two neutral faces) was
modeled as the baseline level of activity and therefore, was not included as a regressor.
Motion regressors were also included. 'Acquisition' and 'other' trials were also modeled.
The regressors were convolved with a double-gamma hemodynamic response function
and temporal filtering was applied as well. Temporal derivatives of each the regressors
were also included.
Whole-brain analyses were conducted using FSL FEAT v. 5.98 (FMRIB’s
Software Library, www.fmrib.ox.ac.uk/fsl). Z (Gaussianised T/F) statistic images were
thresholded at the whole-brain level using clusters determined by Z>2.3 and a (corrected)
66

cluster significance threshold of p=0.05 (Worsley, 2001) unless otherwise noted.
Locations reported by FSL were converted into Talairach coordinates by the MNI-to-
Talairach transformation algorithm (Lancaster et al., 2007). These coordinates were used
to determine the nearest gray matter using the Talairach Daemon version 2.4.2 (Lancaster
et al., 2000).
Regions-of-interest (ROI) analyses. Previous research suggests that the lateral
OFC, in particular, plays an important role in reversal learning (Hampshire & Owen,
2006; O'Doherty, Kringelbach, Rolls, Hornak, & Andrews, 2001). Therefore, we
performed ROI analyses to examine whether this OFC sub-region shows different
activities in reversal learning across the conditions. The left and right lateral OFC were
structurally defined using UCLA’s Laboratory of Neuro Imaging LPBA40 atlas (Shattuck
et al., 2008), set at a 0.5 probabilistic threshold.
Given past findings that the amygdala plays a role in reversal learning in
interaction with the OFC (Izquierdo & Murray, 2005; Stalnaker et al., 2007), we
performed ROI analyses for the left and right amygdala. The amygdala was segmented
from each participant’s high resolution structural scan using FreeSurfer
(surfer.nmr.mgh.harvard.edu) and FSL FAST (FMRIB’s Software Library,
www.fmrib.ox.ac.uk/fsl). For each hemisphere for each participant, we examined the
results from each segmenting software and selected the one judged as more accurate for
further manual correction. Next, manual correction of this selected ROI was carried out
and erroneous voxels in non-amygdala regions (e.g., hippocampus, white matter) were
removed. For both ROI analyses, FSL Featquery was used to extract percent signal
change values.
67

We also performed a post-hoc ROI analysis for the clusters within the parietal
cortex, which showed age-related differences in the whole-brain analyses. The parietal
cortex clusters were functionally defined based on the activation clusters showing
significant age group differences in the neutral condition in the whole brain analysis.
This region was further defined using a parietal lobe mask from MNI structural atlas in
order to remove voxels not within the parietal lobe (e.g., superior occipital gyrus).
Functional connectivity analyses. The structurally defined amygdala (defined as
described above) served as a seed region. In addition, a parietal cortex seed region was
functionally defined using a sphere of 3-mm radius surrounding the peak voxel showing
significant age group differences in the neutral condition in the whole brain analysis. To
examine functional connectivity, we applied a beta series correlation analysis (Gazzaley,
Cooney, Rissman, & D'Esposito, 2005; Rissman, Gazzaley, & D'Esposito, 2004). This
allowed us to use trial-to-trial variability to characterize dynamic inter-regional
interactions. First, a new GLM design file was constructed where each reversal trial was
coded as a unique covariate, resulting in up to 39 independent variables (the maximum
number of reversal trials achieved by participants across all three conditions). To reduce
the confounding effects of the global signal change, the mean signal level over all brain
voxels was calculated for each time point and was used as a covariate. The model also
involved additional nuisance regressors for acquisition and 'other' trials. Second, the least
squares solution of the GLM yielded a beta value for each reversal trial for each
individual participant. These beta values were then sorted by conditions. Third, mean
activity (i.e., mean parameter estimates) was extracted for each individual reversal trial
from a seed region. Fourth, for each condition, we computed correlations between the
68

seed’s beta series and the beta series of all other voxels in the brain, thus generating
condition-specific seed correlation maps. Correlation magnitudes were converted into z-
scores using the Fisher's r-to-z transformation. Condition-dependent changes in
functional connectivity were assessed using random-effects analyses, which were
thresholded at the whole-brain level using clusters determined by Z>2.3 and a (corrected)
cluster significance threshold of p=0.05.
Results
FMRI Results
First, we contrasted brain activity during reversal and acquisition in order to
examine the brain regions that are more important for reversal learning than acquisition.
For the rest of the analyses, we contrasted brain activity during the different types of
reversal trials. In these contrasts, there were no differences in the perceptual properties or
the stimulus emotionality (Figure 7B).
Common activation between younger and older adults
Brain regions showing greater activity during reversal than acquisition in
both groups. When collapsed across groups and conditions, reversal compared with
acquisition trials produced increased activity in inferior frontal gyrus/OFC (BA 47),
frontal pole (BA 10), inferior frontal gyrus (BA 9), anterior cingulate cortex (BA 24 and
32) and insula (BA 13). Furthermore, putamen, caudate, thalamus, posterior cingulate
cortex (BA 23 and 30), precentral gyrus (BA 6), superior temporal gyrus (BA 22), and
inferior parietal lobule (BA 40) showed increased activity in reversal than acquisition
trials. Thus, consistent with previous research (e.g., Ghahremani, Monterosso, Jentsch,
Bilder, & Poldrack, 2010; Kringelbach & Rolls, 2003; Rolls & Grabenhorst, 2008;
69

Tsuchida, Doll, & Fellows, 2010), the OFC and the frontal pole showed greater activity
during reversal than acquisition trials, indicating a critical role of these regions in reversal
learning. There were no age group differences in this contrast, suggesting that younger
and older adults produced similar activity during reversal compared with acquisition
trials.
Brain regions showing different activity during emotional vs. neutral reversal
learning in both groups. Next, we examined whether reversal learning in the positive
and negative emotion conditions produce different patterns of brain activity than reversal
learning in the neutral condition across younger and older adults. The analyses below
were conducted collapsing across groups. The whole-brain analysis revealed greater
activity in the negative than neutral conditions in inferior frontal gyrus/OFC (BA 47),
frontal pole (BA 10), superior frontal gyrus (BA 9) and anterior cingulate (ACC; BA 32).
Other regions showing significant differences in the negative-neutral contrast are reported
in Table 4. There were no significant findings in other contrasts (negative-positive,
positive-negative, positive-neutral, neutral-positive, neutral-negative). However, when
we used a lower threshold (a voxel-threshold of z = 2.3), the positive-neutral contrast
yielded similar results to the ones in the negative-neutral contrast. Compared with the
neutral condition, the positive condition produced greater activity in inferior frontal
gyrus/OFC (BA 47; Figure 5B), frontal pole (BA 10), and ACC (BA 32). Although these
results based on use of a lower threshold should be interpreted with caution, they provide
useful information about the similarities between the positive and negative conditions in
contrast with the neutral condition. Next, the positive and negative conditions (together
called the emotion condition) were combined and contrasted against the neutral
70

condition. The emotion condition yielded greater activity in areas including inferior
frontal gyrus/OFC (BA 47), frontal pole (BA 10), and ACC (BA 32) than did the neutral
condition, whereas the reverse contrast showed no significant findings (Table 4; Figure
8C & D). No age group differences were found in any of the regions mentioned above.
ROI analysis for the OFC. A 2 (group: younger, older) x 3 (condition:
conditions: positive, negative, neutral) mixed analysis of variance (ANOVA) was
performed on the percent signal change from the left and right lateral OFC. There was a
significant effect of condition in the left lateral OFC, F(2, 68) = 11.08, MSE = 0.03, p <
.001, η
p
2
= .25, whereas there was no significant effect of group (p =.19) and no
significant interaction between group and condition (p =.30). Post-hoc t-tests suggest
that the left lateral OFC showed significantly greater activity in the negative than the
neutral conditions, t(35) = 4.46, p < .001, and in the positive than the neutral conditions,
t(35) = 3.16, p = .003, whereas there was no significant difference between the negative
and the positive conditions (p = .18; see Figure 6). These results suggest that the left
lateral OFC is more involved in emotional reversal learning than in neutral reversal
learning in both younger and older adults. For the right OFC, there was a significant
effect of group (M
younger
= -.002; M
older
= .10), F(1, 34) = 4.38, MSE = 0.07, p = .04, η
p
2
=
.11, but no other findings. Across conditions, older adults recruited the right lateral OFC
more than did younger adults, but no differences between conditions were found.
ROI analysis for the amygdala. We conducted 2 (group: younger, older) x 3
(conditions: conditions: positive, negative, neutral) mixed ANOVAs on the percent signal
change from the left and right amygdala. There was a significant effect of condition in
the left amygdala, F(2, 68) = 3.48, MSE = 0.15, p = .04, η
p
2
= .09. A post-hoc t-test
71

suggests that the left amygdala showed significantly greater activity in the negative than
the neutral conditions, t(35) = 2.71, p = .01 (Figure 6). The right amygdala showed a
similar pattern, although the result was marginally significant, F(2, 68) = 2.94, MSE =
0.15, p = .06, η
p
2
= .08. The right amygdala also showed significantly greater activity in
the negative than the neutral conditions, t(35) = 2.19, p = .04. No age group differences
were found in any of these analyses.
Functional connectivity analysis with the amygdala as a seed region. A whole-
brain connectivity analysis with the left amygdala as a seed region was conducted for
each condition. The negative condition produced a significant inverse correlation
between the left amygdala and the right middle frontal gyrus/frontal pole (BA 9, 10;
Figure 7) whereas such negative correlations were not observed in the positive and
neutral conditions (Table 5). The same analysis with the right amygdala as a seed region
did not show negative correlations with the frontopolar regions in any of the conditions.
No age differences were found in any of these analyses.
Age-related differences in brain activity during reversal learning
Although no age-related differences were observed in the frontopolar OFC and
the amygdala, the whole-brain analyses for the negative-neutral and neutral-negative
contrasts revealed age differences in the inferior parietal lobule (BA 40), superior
temporal gyrus (BA 39, 42), precuneus (BA 7), precentral gyrus (BA 6) and postcentral
gyrus (BA 3). Similarly, significant age differences were found for the emotion-neutral
and neutral-emotion contrasts in inferior parietal lobule (BA 40) and superior temporal
gyrus (BA 39, 42). To better identify the nature of these age by emotion interactions, we
directly compared younger and older adults in each of the three emotion conditions. The
72

positive and negative conditions did not produce significant age differences in any of the
brain regions. In contrast, in the neutral condition, older adults showed greater activity in
the inferior parietal lobule (BA 40), superior temporal gyrus (BA 41, 42), precentral
gyrus (BA 4, 6) and superior occipital gyrus (BA 19) than did younger adults.
To further investigate the age differences observed above, we conducted an ROI
analysis for the parietal cortex, which contained most of the clusters showing significant
age group differences (see Figure 8). A one-way ANOVA (comparing positive, negative,
and neutral conditions) on the percent signal change from the parietal cortex revealed a
main effect of group, F(1, 34) = 5.25, MSE = 0.07, p = .03, η
p
2
= .13, and a significant
interaction between group and condition, F(2, 68) = 6.59, MSE = 0.04, p = .002, η
p
2
= .16
(Figure 8). While older adults showed greater parietal cortex activity than younger adults
in the neutral condition, t(34) = 5.20, p < .001, there were no significant group
differences in the negative and positive conditions (p = .66 and p = .42, respectively).
Within-group analyses suggested that older adults exhibited similar parietal cortex
activity across conditions, F(2, 36) = 1.00, MSE = 0.03, p = .38, η
p
2
= .05, whereas
younger adults showed different patterns of activity between conditions, F(2, 32) = 5.67,
MSE = 0.06, p = .01, η
p
2
= .26. Younger adults showed greater activity in the parietal
cortex in the negative than neutral conditions, t(16) = 4.01, p = .001, and in the positive
than neutral conditions, t(16) = 2.32, p = .03.
To further examine the nature of age-related differences in the parietal cortex,
functional connectivity analysis was conducted using the parietal cortex as a seed region.
Older adults showed a significantly greater positive correlation between the parietal
cortex and the anterior cingulate cortex (ACC) than did younger adults in the neutral
73

condition (Table 6). Since the ACC is a critical region for reversal learning (see the
results of the whole brain analysis contrasting reversal vs. acquisition), the greater
positive correlation between the parietal cortex and the ACC may indicate greater effort
made by older than younger adults.
Behavioral Results
The errors made in the first trial of each condition were excluded, as those were
guessing errors and were not due to failure of learning previous associations. The rest of
the errors were divided into two types: reversal and other. The total number of reversal
errors was calculated for each condition. A 2 (group: younger, older) x 3 (conditions:
positive, negative, neutral) mixed analysis of variance (ANOVA) revealed no significant
finings. There were no significant differences between groups (p = .71) and conditions (p
= .68). No significant interaction between group and condition was found (p = .23).
Similarly, there were no significant findings in the total number of other errors between
groups (p = .21) and among conditions (p = .08). No significant interaction between
group and condition was found (p = .46).
However, when we compared reaction time of younger and older adults, we found
age-related differences consistent with the results from the whole brain analysis described
above. To examine how quickly participants responded to the correct face after making
reversal errors, for each condition we computed the average reaction time for trials
immediately following each reversal trial. A 2 (group) x 3 (conditions) ANOVA
revealed no significant findings. However, independent samples t-tests revealed a
significant difference between groups in the neutral condition (M
younger
= .72 sec; M
older
=
.82 sec), t(34) = 2.56 p = .02, but not in the positive (p = .69) and negative conditions (p
74

= .32). In addition, paired samples t-tests suggested that older adults showed a
significantly faster reaction time in the negative than neural conditions (M
negative
= .74
sec; M
neutral
= .82 sec), t(18) = -3.03, p = .01, and the positive than neutral conditions
(M
positive
= .73 sec; M
neutral
= .82 sec), t(18) = 2.63, p = .02, whereas no difference was
found between the negative and positive conditions (p = .53). In contrast, younger adults
showed no significant differences in reaction time in any of these comparisons. Together
with the fMRI results, older adults’ slower reaction time in the neutral condition may
reflect greater effort than in the other conditions and compared with younger adults.
Discussion
This study aimed to examine whether neural mechanisms underlying emotional
memory updating would be similar between younger and older adults. Our results
demonstrated that across age groups, emotional reversal learning produced greater
activity in the OFC and the frontal pole than did neutral reversal learning. The
frontopolar/OFC activity did not significantly differ between younger and older adults
during emotional reversal learning. Consistent with previous research suggesting that the
amygdala remains relatively intact with age, both groups showed significantly greater
activity in the amygdala during negative than neutral reversal learning. Furthermore,
both groups showed negative correlations between the amygdala and the middle frontal
gyrus/frontal pole (BA 9/10) during negative reversal learning. Past research revealed
that the frontal pole has negative correlations with the amygdala when updating old
emotional memories (Finger et al., 2008; Sakaki et al., 2011). Our findings are consistent
with those previous results, and suggest that the frontopolar OFC helps update old
associations by down-regulating the amygdala’s protection of old representations
75

(Schoenbaum, Saddoris, & Stalnaker, 2007; Stalnaker et al., 2007). In addition,
dorsolateral prefrontal cortex, which includes BA 9, was previously implicated in the
control of attention during reversal learning (Hornak et al., 2004); thus, it is possible that
this region also plays a role in down-regulating the amygdala. Importantly, our results
suggest that this mechanism applies to both younger and older adults.
In contrast with emotional reversal learning, neutral reversal learning produced
age-related differences in the parietal cortex, such that older adults showed greater
parietal cortex activity than did younger adults. Previous research suggests that the
ventral parietal cortex reflects bottom-up attention processes elicited by the retrieval cues
or by behaviorally relevant stimuli, especially when they are unexpected (Cabeza,
Ciaramelli, Olson, & Moscovitch, 2008; Cabeza et al., 2011; Corbetta & Shulman, 2002).
The ventral parietal cortex overlaps with most of the regions showing significant age
differences in our study; thus, one possibility is that older compared with younger adults
paid greater attention to the cue that signaled a reversal of a correct face, which occurred
unexpectedly to the participants. Our results also suggested that older versus younger
adults showed greater positive correlations between the parietal cortex and ACC in the
neutral condition. Since the ACC is involved in reversal learning (as shown in the results
from the reversal-acquisition contrast), the stronger parietal cortex -ACC correlations
may suggest that older adults exerted additional effort in updating neutral information.
One hypothesis for the observed age differences is that neutral reversal learning
required more effort for older than for younger adults, resulting in compensatory
recruitment in the parietal cortex regions. In fact, this is consistent with our behavioral
finding that older adults’ reaction time was slower than that of younger adults only in the
76

neutral condition. Furthermore, within-group analyses found that older adults had slower
reaction time in both the negative vs. neutral conditions and in the positive vs. neutral
conditions, suggesting that neutral reversal learning might have been particularly difficult
for older adults. Age-related compensatory recruitment in the parietal cortex was
previously seen in a study using a response inhibition task (Nielson, Langenecker, &
Garavan, 2002), a high-conflict no-go task (Vallesi, McIntosh, & Stuss, 2011) and a
modified version of the physical–numerical interference paradigm task (Huang, Polk,
Goh, & Park, 2012). All of these tasks involved inhibitory control and used only neutral
stimuli, as in the neutral condition of our current study. Thus, it seems possible that older
adults’ parietal cortex activity observed in the current study also reflects age-related
compensatory recruitment.
Several questions remain to be addressed in future studies. First, it is unclear why
we did not observe negative correlations between the amygdala and the frontopolar
regions in the positive condition, unlike that seen in the negative condition. One possible
explanation is that positive reversal learning did not evoke as strong an emotional
response as did negative reversal learning; therefore, reversals of positive associations
required less frontal involvement to modulate old representations in the amygdala than
did reversals of negative associations. In fact, our ROI results suggest that bilateral
amygdala showed less activity during positive than negative reversal learning in both
groups (albeit non-significant); this might suggest that positive reversal learning requires
fewer resources to down-regulate the amygdala than does negative reversal learning.
Second, a question remains with regard to the effects of emotional valence on memory
updating in older adults. Previous research using a similar task (Nashiro, Mather,
77

Gorlick, & Nga, 2011) found that older adults made significantly more errors in the
negative than positive conditions, which was not seen in the current study. One possible
explanation is that the tasks used in this study were easier than the ones in the previous
study, so that increasing task difficulty in the present study would have led to similar
behavioral results to those in the previous study. Future studies should investigate this
discrepancy.
In summary, the current study provides new information about age-related
similarities and differences in the neural mechanisms of memory updating. Our results
suggest that younger and older adults activate similar brain regions during emotional (in
contrast to neutral) reversal learning. This is consistent with previous findings suggesting
that the effects of emotional arousal on memory remain similar between younger and
older adults. In addition, we found age group differences in parietal cortex activity only
during neutral memory updating; this is in line with previous reports on age-related
compensatory recruitment in parietal regions during inhibitory control tasks. Since the
current study employed relatively easy tasks, future studies should investigate whether
increasing task difficulty would affect the observed neural mechanisms underlying
emotional vs. neutral memory updating in both age groups. This line of research is
particularly important for older adults who experience daily challenges in memory
updating, and future research should help us better understand when and how emotion
interacts with our daily learning.
78

Figure 4. Experimental Procedure. The positive (top), negative (middle) or neutral
blocks (bottom) were assigned to the participant in a random order. The two people were
randomly assigned to the right or the left of the screen. The trial began with a
presentation of two people displaying neutral expressions during which the participant
had to select one person by pressing a key. Feedback was presented for 1 sec, which was
followed by a fixation cross for the remainder of the 6 sec. A) In Acquisition Trials
where the response was correct, the selected face changed (into a happy face, angry face,
or face with eyeglasses respectively), while the other face remained neutral. B) In
Reversal Learning Trials where the response was incorrect, both of the faces remained
neutral. Across conditions, the task for the subject was to keep track of the correct person
because it switched mid-game. The correct person changed after several (between three
and six) consecutive correct trials; the number of trials before the change was unknown to
the subject.

79

Figure 4, Continued

80

Figure 5. Brain Regions Showing Differences between Conditions during Reversal
Learning across Groups
The frontal pole and OFC showed similar activity between younger and older adults. The
results shown here are collapsed across groups. A) The frontal pole and OFC showed
greater activity when participants reversed negative associations than neutral associations.
B) The positive-neutral contrast also showed a similar pattern of frontopolar OFC activity
when a lower threshold (a voxel-threshold of z = 2.3) was used. Although the low-
threshold map should be interpreted with caution, it provides useful information about the
similarities between the positive and negative conditions in contrast to the neutral
condition. C) When positive and negative conditions were combined, the emotion
condition showed greater activity in the frontal pole and OFC than did the neutral
condition, D) whereas the reverse contrast showed no significant findings. The images
were threshholded at the whole-brain level using clusters determined by z > 2.3 and a
(corrected) cluster significance threshold of p = 0.05, except for image B.

z = 8

z = 2.3
R
C) Emotion - Neutral
A) Negative - Neutral
z = -14
D) Neutral - Emotion
B) Positive - Neutral
R
81

Figure 6. Brain Activity in the Left Lateral OFC and the Left Amygdala during Reversal
Learning across Conditions
Younger and older adults showed similar patterns of activity in (A) the left lateral OFC
and (B) the left amygdala across conditions. Collapsed across groups, participants
showed significantly greater activity in the negative than neutral conditions and the
positive than neutral conditions, although the positive-neutral contrast for the left
amygdala did not reach a significant level.

A) The Left Lateral OFC
B) The Left Amygdala
82

Figure 7. Regions Showing Negative Connectivity with the Left Amygdala across Groups
Collapsed across groups, the left amygdala showed negative functional connectivity with
the right middle frontal gyrus (BA 9) and frontal pole (BA 10) in the negative condition.
The image was threshholded at the whole-brain level using clusters determined by z > 2.3
and a (corrected) cluster significance threshold of p = .05.

R
z = 20
83

Figure 8. Brain Activity in the Parietal Cortex Showing Age-related Differences in the
Neutral Condition
The left image shows age-related differences in the parietal cortex in the neutral
condition. Older adults showed greater parietal cortex activity than did younger adults.
The image was threshholded at the whole-brain level using clusters determined by z > 2.3
and a (corrected) cluster significance threshold of p = .05. The bar graph on the right
shows the mean % signal change in the bilateral parietal cortex, revealing different
patterns of parietal cortex activity between younger and older adults in the neutral
condition.

s

R
z = 30
84

Table 4. Brain Activity Showing Significant Differences between Conditions during
Reversal Learning in Younger and Older Adults.

MNI Talairach
Area H BA x y z x y z Z-max
Negative > Neutral
Putamen L -26 -2 6 -25 -4 9 3.71
Putamen L -32 -2 4 -31 -4 7 3.41
Inferior Frontal Gyrus L 47 -52 20 -14 -49 18 -7 3.34
Middle Occipital Gyrus L 18 -22 -94 14 -22 -90 8 3.45
Fusiform Gyrus L 37 -48 -54 -2 -46 -52 -3 3.45
Middle Occipital Gyrus L 19 -26 -92 16 -25 -89 10 3.35
Cuneus L 17 -8 -84 12 -9 -81 7 3.2
Posterior Cingulate L 31 -6 -38 32 -7 -40 29 3.2
Culmen L -4 -72 -2 -5 -69 -4 3.16
Anterior Cingulate L 32 -2 44 -20 -3 41 -10 3.37
Superior Frontal Gyrus/
Frontal pole R 9/10 4 70 18 3 62 26 3.29
Anterior Cingulate L 32 -2 44 -10 -3 40 -1 3.29
Inferior Frontal Gyrus R 47 56 22 -8 51 19 0 3.25
Inferior Frontal Gyrus R 47 52 22 -14 47 20 -6 3.23
Claustrum R 38 16 -8 34 14 -1 3.03
Superior Temporal Gyrus R 42 66 -30 16 60 -31 17 3.19
Superior Temporal Gyrus R 42 58 -34 12 52 -35 13 3.07
Middle Temporal Gyrus R 21 66 -22 -6 60 -22 -2 3.02
Thalamus L -6 -24 -4 -7 -24 -2 3.53
Thalamus L -6 -24 0 -7 -24 2 3.4
Thalamus L -8 -22 4 -9 -23 6 3.29
Positive > Neutral No significant results
Negative > Positive No significant results
Positive > Negative No significant results
Neutral > Negative No significant results
Neutral > Positive No significant results
85

Table 4, Continued
Emotion > Neutral
Fusiform Gyrus L 37 -48 -54 -2 -46 -52 -3 3.37
Fusiform Gyrus L 37 -58 -56 6 -55 -54 4 3.24
Middle Temporal Gyrus L 21 -68 -20 -10 -64 -19 -8 3.15
Lingual Gyrus L -6 -84 8 -7 -81 4 3.33
Cuneus R 18 6 -78 14 4 -76 10 3.06
Culmen L -4 -72 -2 -5 -69 -4 3.02
Inferior Frontal Gyrus L 47 -36 32 -4 -34 29 3 3.31
Inferior Frontal Gyrus L 47 -52 20 -14 -49 18 -7 3.28
Inferior Frontal Gyrus L 47 -44 28 -12 -42 26 -5 3.22
Anterior Cingulate L 32 -2 44 -20 -3 41 -10 3.57
Anterior Cingulate L 32 -2 46 -12 -3 42 -3 3.4
Frontal pole R 10 2 66 -12 1 61 -1 3.19
Neutral > Emotion
No significant results
86

Table 5. Brain Regions Showing Negative Connectivity with the Left Amygdala across
Groups.

MNI Talairach
Area H BA x y z x y z Z-max
Negative
Inferior Parietal Lobule R 40 48 -48 44 44 -49 40 3.97
Inferior Parietal Lobule R 40 48 -50 52 44 -52 47 3.87
Inferior Parietal Lobule R 40 40 -44 38 37 -45 35 3.86
Middle Frontal Gyrus R 9 42 18 38 39 13 39 5.16
Middle Frontal Gyrus R 9 44 24 36 41 19 37 4.68
Frontal pole R 10 32 60 20 29 54 25 4.56
Precuneus R 7 8 -72 50 6 -72 44 4.61
Precuneus R 7 6 -56 64 4 -58 57 4.12
Precuneus R 7 -18 -78 50 -19 -78 43 3.46
Positive
Precuneus R 7 18 -78 52 16 -78 45 3.92
Precuneus R 31 6 -74 28 4 -73 24 3.76
Precuneus R 7 14 -78 52 12 -78 45 3.74
Neutral
Precuneus R 7 -4 -80 50 -5 -80 43 4.18
Cuneus R 19 2 -82 44 0 -81 38 4.08
Cuneus R 18 2 -76 36 0 -75 31 3.84

87

Table 6. Brain Regions Showing Age-related Differences in Positive Connectivity with
the Parietal Cortex.

MNI Talairach
Area H BA x y z x y z Z-max
Older - Younger
Thalamus R 8 -8 18 6 -10 19 4.28
Anterior Cingulate L 33 2 22 12 1 19 15 4.1
Cingulate Gyrus L 31 -20 -46 32 -20 -46 29 4.06
Anterior Cingulate R 32 24 34 12 22 30 16 3.58
Middle Frontal Gyrus R 8 30 12 36 27 8 37 3.49
Anterior Cingulate R 32 24 14 28 22 10 29 3.44
Younger - Older
Insula R 13 44 4 -2 41 3 2 4.7
Insula R 13 40 12 6 37 10 10 4.66
Claustrum R 36 8 6 33 6 9 4.49
Precentral Gyrus L 44 -64 12 0 -62 11 4 3.82
Superior Temporal Gyrus L 22 -56 12 0 -54 11 4 3.63
Insula L 13 -42 0 0 -41 -1 3 3.53

88

CONCLUSION
In Chapter 1, three experiments were conducted to examine the effects of
emotional arousal on associative memory in older adults. Older adults, both with and
without AD, showed better associative memory for emotional than neutral items when
the task was relatively easy. The results suggest that emotional arousal can enhance
associative memory in older adults, but task difficulty plays a role in whether they benefit
from emotional content. One possible explanation is that since older adults have
associative memory deficits to begin with, they may need more exposure to stimuli than
younger adults to show arousal enhancement in associative memory.
While Chapter 1 examined how emotion affects associative memory for novel
items, Chapter 2 investigated the effects of emotion on associative memory for
previously-encountered items. Prior research suggested that younger adults had more
difficulty updating emotional than neutral associative memories (Mather & Knight, 2008;
Novak & Mather, 2009). Chapter 2 examined whether the same phenomenon would
apply to older adults and indeed found that older adults showed a similar emotion
impairing effect on associative memory updating. One possible explanation is that old
associative memory with high emotional salience may be equally important as new
associative memory with the same emotional information, which creates a competition
between old and new memories. This idea is consistent with arousal-biased competition
theory (Mather & Sutherland, 2011)(Mather & Southerland, 2011), suggesting that
emotional arousal enhances associative memory when there is no other competing high-
priority information whereas arousal has an opposite negative effect when multiple high-
89

priority targets compete for attention, resulting in diminished associative memory for
each target.
Chapter 3 investigated brain mechanisms underlying emotional vs. neutral
associative memory updating in younger and older adults. This study used easy tasks in
order to avoid potential confounds of the effect of task difficulty on brain activation
patterns. As expected, the behavioral data revealed no age-group differences and showed
that both younger and older adults performed near ceiling. However, the fMRI results
revealed interesting within- and between-group differences in neural activity during
memory updating tasks. Both younger and older adults showed greater activity in the
OFC and the frontal pole during emotional than neutral reversal learning. Moreover,
both groups showed similar negative interactions between the amygdala and the middle
frontal gyrus/frontal pole regions during negative reversal learning. In contrast, age-
group differences were observed during neutral memory updating, such that older adults
showed greater parietal cortex activity than did younger adults. Although no a priori
hypothesis was made regarding age-related differences during neutral memory updating,
the results raised an interesting possibility that older adults’ additional parietal activity
may reflect compensatory recruitment.
In summary, this study suggests that emotional arousal can enhance or impair
associative memory in a similar manner in younger and older adults. Furthermore, the
fMRI results revealed that the frontopolar OFC regions and the amygdala activate
similarly in both age groups. Interestingly, the results also showed age-group differences
in brain activity when associative learning does not involve emotion. The observed age
differences in parietal cortex activity may reflect how associative information is
90

processed differently between younger and older individuals in everyday learning
situations, leading to poor associative learning in older adults. On the other hand,
associative learning involving emotional content seems to minimize the difference
between younger and older adults.
Several limitations should be addressed in future research. In this study, emotion
enhancement in associative memory was observed only when tasks were made easy. The
fMRI study also used easy tasks and found similar brain activity between younger and
older adults during emotional memory updating. It is possible that increasing task
difficulty leads to more complex patterns of brain activity, which may differ between
younger and older adults. Future studies should examine more precise roles of task
difficulty in emotion-memory interactions.
Despite the fact that several questions remain, the current study provides
important new information about how emotional arousal influences associative learning
in older adults. When task demands are low, emotional arousal modulates associative
memory in a similar way in younger and older adults. This seems to be due to good
structural and functional preservation of the amygdala in old age. Interesting future
research would be to investigate possible ways to use preserved amygdala networks to
improve older adults’ memory and learning. For example, it would be interesting to
incorporate emotional feedback into cognitive training programs in order to make
training more effective and enjoyable. As mentioned in the beginning of this paper, age-
related memory decline is associated with many other negative health outcomes. Thus,
finding ways to improve associative memory – a type of memory severely affected by
age – is essential for future studies. A combination of behavioral and neuroimaging
91

methods should allow us to further investigate when and how factors, such as emotion,
modulate associative memory in beneficial or harmful ways. This line of research is
critical for developing effective learning strategies for older adults.
92

REFERENCES
Abrisqueta-Gomez, J., Bueno, O. F., Oliveira, M. G., & Bertolucci, P. H. (2002).
Recognition memory for emotional pictures in Alzheimer's patients. Acta Neurol
Scand, 105(1), 51-54.
Achim, A. M., & Lepage, M. (2005). Neural correlates of memory for items and for
associations: an event-related functional magnetic resonance imaging study. J
Cogn Neurosci, 17(4), 652-667. doi: 10.1162/0898929053467578
Allen, J. S., Bruss, J., Brown, C. K., & Damasio, H. (2005). Normal neuroanatomical
variation due to age: the major lobes and a parcellation of the temporal
region.Neurobiol Aging, 26(9), 1245-1260; discussion 1279-1282. doi:
10.1016/j.neurobiolaging.2005.05.023
Anderson, L., & Shimamura, A. P. (2005). Influences of emotion on context memory
while viewing film clips. Am J Psychol, 118(3), 323-337.
Bartzokis, G., Beckson, M., Lu, P. H., Nuechterlein, K. H., Edwards, N., & Mintz, J.
(2001). Age-related changes in frontal and temporal lobe volumes in men: a
magnetic resonance imaging study. Arch Gen Psychiatry, 58(5), 461-465.
Beckmann, C. F., & Smith, S. M. (2004). Probabilistic independent component analysis
for functional magnetic resonance imaging. IEEE Trans Med Imaging, 23(2),
137-152. doi: 10.1109/TMI.2003.822821
Blackwell, A. D., Sahakian, B. J., Vesey, R., Semple, J. M., Robbins, T. W., & Hodges, J.
R. (2004). Detecting dementia: novel neuropsychological markers of preclinical
Alzheimer's disease. Dement Geriatr Cogn Disord, 17(1-2), 42-48. doi:
10.1159/000074081
93

Brabec, J., Rulseh, A., Hoyt, B., Vizek, M., Horinek, D., Hort, J., & Petrovicky, P. (2010).
Volumetry of the human amygdala - an anatomical study. Psychiatry Res, 182(1),
67-72. doi: 10.1016/j.pscychresns.2009.11.005
Bucks, R. S., & Radford, S. A. (2004). Emotion processing in Alzheimer's disease. Aging
Ment Health, 8(3), 222-232. doi: 10.1080/13607860410001669750
Budson, A. E., Todman, R. W., Chong, H., Adams, E. H., Kensinger, E. A., Krangel, T.
S., & Wright, C. I. (2006). False recognition of emotional word lists in aging and
Alzheimer disease. Cogn Behav Neurol, 19(2), 71-78. doi:
10.1097/01.wnn.0000213905.49525.d0
Cabeza, R., Ciaramelli, E., Olson, I. R., & Moscovitch, M. (2008). The parietal cortex
and episodic memory: an attentional account. Nat Rev Neurosci, 9(8), 613-625.
doi: 10.1038/nrn2459
Cabeza, R., Mazuz, Y. S., Stokes, J., Kragel, J. E., Woldorff, M. G., Ciaramelli, E., . . .
Moscovitch, M. (2011). Overlapping parietal activity in memory and perception:
evidence for the attention to memory model. J Cogn Neurosci, 23(11), 3209-3217.
doi: 10.1162/jocn_a_00065
Canli, T., Desmond, J. E., Zhao, Z., & Gabrieli, J. D. (2002). Sex differences in the
neural basis of emotional memories. Proc Natl Acad Sci U S A, 99(16), 10789-
10794. doi: 10.1073/pnas.162356599
Chalfonte, B. L., & Johnson, M. K. (1996). Feature memory and binding in young and
older adults. Mem Cognit, 24(4), 403-416.
94

Charles, S. T., Mather, M., & Carstensen, L. L. (2003). Aging and emotional memory:
the forgettable nature of negative images for older adults. J Exp Psychol Gen,
132(2), 310-324.
Chee, M. W., Goh, J. O., Venkatraman, V., Tan, J. C., Gutchess, A., Sutton, B., . . . Park,
D. (2006). Age-related changes in object processing and contextual binding
revealed using fMR adaptation. J Cogn Neurosci, 18(4), 495-507. doi:
10.1162/jocn.2006.18.4.495
Cook, G. I., Hicks, J. L., & Marsh, R. L. (2007). Source monitoring is not always
enhanced for valenced material. Mem Cognit, 35(2), 222-230.
Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven
attention in the brain. Nat Rev Neurosci, 3(3), 201-215. doi: 10.1038/nrn755
Cowan, N., Naveh-Benjamin, M., Kilb, A., & Saults, J. S. (2006). Life-span development
of visual working memory: when is feature binding difficult? Dev Psychol, 42(6),
1089-1102. doi: 10.1037/0012-1649.42.6.1089
Daselaar, S. M., Fleck, M. S., Dobbins, I. G., Madden, D. J., & Cabeza, R. (2006).
Effects of healthy aging on hippocampal and rhinal memory functions: an event-
related fMRI study. Cereb Cortex, 16(12), 1771-1782. doi: 10.1093/cercor/bhj112
Davachi, L., & Wagner, A. D. (2002). Hippocampal contributions to episodic encoding:
insights from relational and item-based learning. J Neurophysiol, 88(2), 982-990.
Davidson, P. S., McFarland, C. P., & Glisky, E. L. (2006). Effects of emotion on item
and source memory in young and older adults. Cogn Affect Behav Neurosci, 6(4),
306-322.
95

Denburg, N. L., Buchanan, T. W., Tranel, D., & Adolphs, R. (2003). Evidence for
preserved emotional memory in normal older persons. Emotion, 3(3), 239-253.
doi: 10.1037/1528-3542.3.3.239
Doerksen, S., & Shimamura, A. P. (2001). Source memory enhancement for emotional
words. Emotion, 1(1), 5-11.
Ebner, N. C., Riediger, M., & Lindenberger, U. (2010). FACES--a database of facial
expressions in young, middle-aged, and older women and men: development and
validation. Behav Res Methods, 42(1), 351-362. doi: 10.3758/BRM.42.1.351
Finger, E. C., Mitchell, D. G. V., Jones, M., & Blair, R. J. R. (2008). Dissociable roles of
medial orbito-frontal cortex in human operant extinction learning. Neuroimage,
43, 748–755. doi: 10.1016/j.neuroimage.2008.08.021
Fjell, A. M., Westlye, L. T., Amlien, I., Espeseth, T., Reinvang, I., Raz, N., . . . Walhovd,
K. B. (2009). High consistency of regional cortical thinning in aging across
multiple samples. Cereb Cortex, 19(9), 2001-2012. doi: 10.1093/cercor/bhn232
Fowler, K. S., Saling, M. M., Conway, E. L., Semple, J. M., & Louis, W. J. (2002).
Paired associate performance in the early detection of DAT. J Int Neuropsychol
Soc, 8(1), 58-71.
Gazzaley, A., Cooney, J. W., Rissman, J., & D'Esposito, M. (2005). Top-down
suppression deficit underlies working memory impairment in normal aging. Nat
Neurosci, 8(10), 1298-1300. doi: 10.1038/nn1543
Ghahremani, D. G., Monterosso, J., Jentsch, J. D., Bilder, R. M., & Poldrack, R. A.
(2010). Neural components underlying behavioral flexibility in human reversal
learning. Cereb Cortex, 20, 1843–1852. doi: 10.1093/cercor/bhp247
96

Goh, J. O., Chee, M. W., Tan, J. C., Venkatraman, V., Hebrank, A., Leshikar, E. D., . . .
Park, D. C. (2007). Age and culture modulate object processing and object-scene
binding in the ventral visual area. Cogn Affect Behav Neurosci, 7(1), 44-52.
Grady, C. L., McIntosh, A. R., Horwitz, B., Maisog, J. M., Ungerleider, L. G., Mentis, M.
J., . . . Haxby, J. V. (1995). Age-related reductions in human recognition memory
due to impaired encoding. Science, 269(5221), 218-221.
Hadley, C. B., & Mackay, D. G. (2006). Does emotion help or hinder immediate
memory? Arousal versus priority-binding mechanisms. J Exp Psychol Learn Mem
Cogn, 32(1), 79-88. doi: 10.1037/0278-7393.32.1.79
Hampshire, A., & Owen, A. M. (2006). Fractionating attentional control using event-
related fMRI. Cereb Cortex, 16(12), 1679-1689. doi: 10.1093/cercor/bhj116
Hoefer, M., Allison, S. C., Schauer, G. F., Neuhaus, J. M., Hall, J., Dang, J. N., . . . Rosen,
H. J. (2008). Fear conditioning in frontotemporal lobar degeneration and
Alzheimer's disease. Brain, 131(Pt 6), 1646-1657. doi: 10.1093/brain/awn082
Hornak, J., O'Doherty, J., Bramham, J., Rolls, E. T., Morris, R. G., Bullock, P. R., &
Polkey, C. E. (2004). Reward-related reversal learning after surgical excisions in
orbito-frontal or dorsolateral prefrontal cortex in humans. J Cogn Neurosci, 16(3),
463-478. doi: 10.1162/089892904322926791
Huang, C. M., Polk, T. A., Goh, J. O., & Park, D. C. (2012). Both left and right posterior
parietal activations contribute to compensatory processes in normal aging.
Neuropsychologia, 50(1), 55-66. doi: 10.1016/j.neuropsychologia.2011.10.022
97

Isaacowitz, D. M., Wadlinger, H. A., Goren, D., & Wilson, H. R. (2006a). Is there an
age-related positivity effect in visual attention? A comparison of two
methodologies. Emotion, 6(3), 511-516. doi: 10.1037/1528-3542.6.3.511
Isaacowitz, D. M., Wadlinger, H. A., Goren, D., & Wilson, H. R. (2006b). Selective
preference in visual fixation away from negative images in old age? An eye-
tracking study. Psychol Aging, 21(1), 40-48. doi: 10.1037/0882-7974.21.1.40
Izquierdo, A., & Murray, E. A. (2005). Opposing effects of amygdala and orbital
prefrontal cortex lesions on the extinction of instrumental responding in macaque
monkeys. Eur J Neurosci, 22(9), 2341-2346. doi: 10.1111/j.1460-
9568.2005.04434.x
John, J. P., Burgess, P. W., Yashavantha, B. S., Shakeel, M. K., Halahalli, H. N., & Jain,
S. (2009). Differential relationship of frontal pole and whole brain volumetric
measures with age in neuroleptic-naive schizophrenia and healthy subjects.
Schizophr Res, 109(1-3), 148-158. doi: 10.1016/j.schres.2008.12.019
Kazui, H., Mori, E., Hashimoto, M., & Hirono, N. (2003). Enhancement of declarative
memory by emotional arousal and visual memory function in Alzheimer's disease.
J Neuropsychiatry Clin Neurosci, 15(2), 221-226.
Kensinger, E. A., Brierley, B., Medford, N., Growdon, J. H., & Corkin, S. (2002). Effects
of normal aging and Alzheimer's disease on emotional memory. Emotion, 2(2),
118-134.
Kensinger, E. A., & Corkin, S. (2003). Memory enhancement for emotional words: are
emotional words more vividly remembered than neutral words? Mem Cognit,
31(8), 1169-1180.
98

Kensinger, E. A., Garoff-Eaton, R. J., & Schacter, D. L. (2007). Effects of emotion on
memory specificity in young and older adults. J Gerontol B Psychol Sci Soc Sci,
62(4), P208-215.
Kensinger, E. A., Gutchess, A. H., & Schacter, D. L. (2007). Effects of aging and
encoding instructions on emotion-induced memory trade-offs. Psychol Aging,
22(4), 781-795. doi: 10.1037/0882-7974.22.4.781
Kensinger, E. A., O'Brien, J. L., Swanberg, K., Garoff-Eaton, R. J., & Schacter, D. L.
(2007). The effects of emotional content on reality-monitoring performance in
young and older adults. Psychol Aging, 22(4), 752-764. doi: 10.1037/0882-
7974.22.4.752
Kensinger, E. A., & Schacter, D. L. (2006). Amygdala activity is associated with the
successful encoding of item, but not source, information for positive and negative
stimuli. J Neurosci, 26(9), 2564-2570. doi: 10.1523/JNEUROSCI.5241-05.2006
Kensinger, E. A., & Schacter, D. L. (2008). Neural processes supporting young and older
adults' emotional memories. J Cogn Neurosci, 20(7), 1161-1173. doi:
10.1162/jocn.2008.20080
Kessels, R. P., Hobbel, D., & Postma, A. (2007). Aging, context memory and binding: a
comparison of "what, where and when" in young and older adults. Int J Neurosci,
117(6), 795-810. doi: 10.1080/00207450600910218
Kilb, A., & Naveh-Benjamin, M. (2007). Paying attention to binding: further studies
assessing the role of reduced attentional resources in the associative deficit of
older adults. Mem Cognit, 35(5), 1162-1174.
99

Knight, M., Seymour, T. L., Gaunt, J. T., Baker, C., Nesmith, K., & Mather, M. (2007).
Aging and goal-directed emotional attention: distraction reverses emotional biases.
Emotion, 7(4), 705-714. doi: 10.1037/1528-3542.7.4.705
Koff, E., Zaitchik, D., Montepare, J., & Albert, M. S. (1999). Emotion processing in the
visual and auditory domains by patients with Alzheimer's disease. J Int
Neuropsychol Soc, 5(1), 32-40.
Kramer, J. H., Rosen, H. J., Du, A. T., Schuff, N., Hollnagel, C., Weiner, M. W., . . .
Delis, D. C. (2005). Dissociations in hippocampal and frontal contributions to
episodic memory performance. Neuropsychology, 19(6), 799-805. doi:
10.1037/0894-4105.19.6.7999
Kringelbach, M. L., & Rolls, E. T. (2003). Neural correlates of rapid reversal learning in
a simple model of human social interaction. Neuroimage, 20, 1371–1383. doi:
10.1016/S1053-8119(03)00393-8
LaBar, K. S., & Cabeza, R. (2006). Cognitive neuroscience of emotional memory. Nat
Rev Neurosci, 7(1), 54-64. doi: 10.1038/nrn1825
Lamar, M., Yousem, D. M., & Resnick, S. M. (2004). Age differences in orbitofrontal
activation: an fMRI investigation of delayed match and nonmatch to sample.
Neuroimage, 21(4), 1368-1376. doi: 10.1016/j.neuroimage.2003.11.018
Lancaster, J. L., Tordesillas-Gutierrez, D., Martinez, M., Salinas, F., Evans, A., Zilles,
K., . . . Fox, P. T. (2007). Bias between MNI and Talairach coordinates analyzed
using the ICBN-152 brain template. Human Brain Mapping, 28(11), 1194-1205.
doi: 10.1002/hbm.20345
100

Lancaster, J. L., Woldorff, M. G., Parsons, L. M., Liotti, M., Freitas, C. S., Rainey, L., . . .
Fox, P. T. (2000). Automated Talairach Atlas labels for functional brain mapping.
Human Brain Mapping, 10(3), 120-131. doi: 10.1002/1097-
0193(200007)10:3<120::AID-HBM30>3.0.CO;2-8
Lavenu, I., Pasquier, F., Lebert, F., Petit, H., & Van der Linden, M. (1999). Perception of
emotion in frontotemporal dementia and Alzheimer disease. Alzheimer Dis Assoc
Disord, 13(2), 96-101.
Leclerc, C. M., & Kensinger, E. A. (2008). Effects of age on detection of emotional
information. Psychol Aging, 23(1), 209-215. doi: 10.1037/0882-7974.23.1.209
Lin, F. R., Ferrucci, L., Metter, E. J., An, Y., Zonderman, A. B., & Resnick, S. M. (2011).
Hearing loss and cognition in the Baltimore Longitudinal Study of Aging.
Neuropsychology, 25(6), 763-770. doi: 10.1037/a0024238
Lindeboom, J., Schmand, B., Tulner, L., Walstra, G., & Jonker, C. (2002). Visual
association test to detect early dementia of the Alzheimer type. J Neurol
Neurosurg Psychiatry, 73(2), 126-133.
Luzzi, S., Piccirilli, M., & Provinciali, L. (2007). Perception of emotions on happy/sad
chimeric faces in Alzheimer disease: relationship with cognitive functions.
Alzheimer Dis Assoc Disord, 21(2), 130-135. doi:
10.1097/WAD.0b013e318064f445
MacKay, D. G., & Ahmetzanov, M. V. (2005). Emotion, memory, and attention in the
taboo Stroop paradigm. Psychol Sci, 16(1), 25-32. doi: 10.1111/j.0956-
7976.2005.00776.x
101

Malmberg, K. J., & Shiffrin, R. M. (2005). The "one-shot" hypothesis for context storage.
J Exp Psychol Learn Mem Cogn, 31(2), 322-336. doi: 10.1037/0278-
7393.31.2.322
Mather, M., & Carstensen, L. L. (2003). Aging and attentional biases for emotional faces.
Psychol Sci, 14(5), 409-415.
Mather, M., Gorlick, M. A., & Nesmith, K. (2009). The limits of arousal's memory-
impairing effects on nearby information. Am J Psychol, 122(3), 349-369.
Mather, M., & Knight, M. (2005). Goal-directed memory: the role of cognitive control in
older adults' emotional memory. Psychol Aging, 20(4), 554-570. doi:
10.1037/0882-7974.20.4.554
Mather, M., & Knight, M. (2008). The emotional harbinger effect: poor context memory
for cues that previously predicted something arousing. Emotion, 8(6), 850-860.
doi: 10.1037/a0014087
Mather, M., & Knight, M. R. (2006). Angry faces get noticed quickly: threat detection is
not impaired among older adults. J Gerontol B Psychol Sci Soc Sci, 61(1), P54-57.
Mather, M., & Nesmith, K. (2008). Arousal-Enhanced Location Memory for Pictures. J
Mem Lang, 58(2), 449-464. doi: 10.1016/j.jml.2007.01.004
Mather, M., & Sutherland, M. R. (2011). Arousal-biased competition in perception and
memory. Perspect Psychol Sci, 6(2), 114-133. doi: 10.1177/1745691611400234
May, C. P., Rahhal, T., Berry, E. M., & Leighton, E. A. (2005). Aging, source memory,
and emotion. Psychol Aging, 20(4), 571-578. doi: 10.1037/0882-7974.20.4.571
102

Mell, T., Heekeren, H. R., Marschner, A., Wartenburger, I., Villringer, A., & Reischies, F.
M. (2005). Effect of aging on stimulus-reward association learning.
Neuropsychologia, 43(4), 554-563. doi: 10.1016/j.neuropsychologia.2004.07.010
Mitchell, K. J., Johnson, M. K., Raye, C. L., & D'Esposito, M. (2000). fMRI evidence of
age-related hippocampal dysfunction in feature binding in working memory.
Brain Res Cogn Brain Res, 10(1-2), 197-206.
Mitchell, K. J., Johnson, M. K., Raye, C. L., Mather, M., & D'Esposito, M. (2000). Aging
and reflective processes of working memory: binding and test load deficits.
Psychol Aging, 15(3), 527-541.
Mitchell, K. J., Raye, C. L., Johnson, M. K., & Greene, E. J. (2006). An fMRI
investigation of short-term source memory in young and older adults. Neuroimage,
30(2), 627-633. doi: 10.1016/j.neuroimage.2005.09.039
Moayeri, S. E., Cahill, L., Jin, Y., & Potkin, S. G. (2000). Relative sparing of emotionally
influenced memory in Alzheimer's disease. Neuroreport, 11(4), 653-655.
Mol, M., Carpay, M., Ramakers, I., Rozendaal, N., Verhey, F., & Jolles, J. (2007). The
effect of perceived forgetfulness on quality of life in older adults; a qualitative
review. Int J Geriatr Psychiatry, 22(5), 393-400. doi: 10.1002/gps.1686
Montejo, P., Montenegro, M., Fernandez, M. A., & Maestu, F. (2011). Subjective
memory complaints in the elderly: Prevalence and influence of temporal
orientation, depression and quality of life in a population-based study in the city
of Madrid. Aging Ment Health, 15(1), 85-96. doi:
10.1080/13607863.2010.501062
103

Montejo, P., Montenegro, M., Fernandez, M. A., & Maestu, F. (2012). Memory
complaints in the elderly: quality of life and daily living activities. A population
based study. Arch Gerontol Geriatr, 54(2), 298-304. doi:
10.1016/j.archger.2011.05.021
Nashiro, K., & Mather, M. (2011a). Effects of emotional arousal on memory binding in
normal aging and Alzheimer's disease. Am J Psychol, 124(3), 301-312.
Nashiro, K., & Mather, M. (2011b). How arousal affects younger and older adults'
memory binding. Exp Aging Res, 37(1), 108-128. doi:
10.1080/0361073X.2011.536746
Nashiro, K., Mather, M., Gorlick, M. A., & Nga, L. (2011). Negative emotional outcomes
impair older adults' reversal learning. Cogn Emot, 25(6), 1014-1028. doi:
10.1080/02699931.2010.542999
Nashiro, K., Sakaki, M., Huffman, D., & Mather, M. (in press). Both younger and older
adults have difficulty updating emotional memories. Journal of Gerontology:
Psychological Sciences.
Nashiro, K., Sakaki, M., & Mather, M. (2012). Age differences in brain activity during
emotion processing: reflections of age-related decline or increased emotion
regulation? Gerontology, 58(2), 156-163. doi: 10.1159/000328465
Nashiro, K., Sakaki, M., Nga, L., & Mather, M. (in press). Differential brain activity
during emotional vs. non-emotional reversal learning. J Cogn Neurosci.
Naveh-Benjamin, M. (2000). Adult age differences in memory performance: tests of an
associative deficit hypothesis. J Exp Psychol Learn Mem Cogn, 26(5), 1170-1187.
104

Naveh-Benjamin, M., Brav, T. K., & Levy, O. (2007). The associative memory deficit of
older adults: the role of strategy utilization. Psychol Aging, 22(1), 202-208. doi:
10.1037/0882-7974.22.1.202
Naveh-Benjamin, M., Guez, J., Kilb, A., & Reedy, S. (2004). The associative memory
deficit of older adults: further support using face-name associations. Psychol
Aging, 19(3), 541-546. doi: 10.1037/0882-7974.19.3.541
Naveh-Benjamin, M., Guez, J., & Shulman, S. (2004). Older adults' associative deficit in
episodic memory: assessing the role of decline in attentional resources. Psychon
Bull Rev, 11(6), 1067-1073.
Neiss, M. B., Leigland, L. A., Carlson, N. E., & Janowsky, J. S. (2009). Age differences
in perception and awareness of emotion. Neurobiol Aging, 30(8), 1305-1313. doi:
10.1016/j.neurobiolaging.2007.11.007
Nielson, K. A., Langenecker, S. A., & Garavan, H. (2002). Differences in the functional
neuroanatomy of inhibitory control across the adult life span. Psychol Aging,
17(1), 56-71.
Novak, D. L., & Mather, M. (2009). The tenacious nature of memory binding for
arousing negative items. Mem Cognit, 37(7), 945-952. doi: 10.3758/MC.37.7.945
O'Connell, H., Coen, R., Kidd, N., Warsi, M., Chin, A. V., & Lawlor, B. A. (2004). Early
detection of Alzheimer's disease (AD) using the CANTAB paired Associates
Learning Test. Int J Geriatr Psychiatry, 19(12), 1207-1208. doi:
10.1002/gps.1180
105

O'Doherty, J., Kringelbach, M. L., Rolls, E. T., Hornak, J., & Andrews, C. (2001).
Abstract reward and punishment representations in the human orbitofrontal cortex.
Nat Neurosci, 4(1), 95-102. doi: 10.1038/82959
Old, S. R., & Naveh-Benjamin, M. (2008). Differential effects of age on item and
associative measures of memory: a meta-analysis. Psychol Aging, 23(1), 104-118.
doi: 10.1037/0882-7974.23.1.104
Olson, I. R., Page, K., Moore, K. S., Chatterjee, A., & Verfaellie, M. (2006). Working
memory for conjunctions relies on the medial temporal lobe. J Neurosci, 26(17),
4596-4601. doi: 10.1523/JNEUROSCI.1923-05.2006
Parra, M. A., Abrahams, S., Fabi, K., Logie, R., Luzzi, S., & Della Sala, S. (2009). Short-
term memory binding deficits in Alzheimer's disease. Brain, 132(Pt 4), 1057-1066.
doi: 10.1093/brain/awp036
Pezdek, K., & Hartman, E. F. (1983). Children's television viewing: attention and
comprehension of auditory versus visual information. Child Dev, 54(4), 1015-
1023.
Pfister, T. D., Reinhold, W. C., Agama, K., Gupta, S., Khin, S. A., Kinders, R. J., . . .
Pommier, Y. (2009). Topoisomerase I levels in the NCI-60 cancer cell line panel
determined by validated ELISA and microarray analysis and correlation with
indenoisoquinoline sensitivity. Mol Cancer Ther, 8(7), 1878-1884. doi:
10.1158/1535-7163.MCT-09-0016
Provyn, J. P., Sliwinski, M. J., & Howard, M. W. (2007). Effects of age on contextually
mediated associations in paired associate learning. Psychol Aging, 22(4), 846-857.
doi: 10.1037/0882-7974.22.4.846
106

Rahhal, T. A., May, C. P., & Hasher, L. (2002). Truth and character: sources that older
adults can remember. Psychol Sci, 13(2), 101-105.
Raz, N., Lindenberger, U., Rodrigue, K. M., Kennedy, K. M., Head, D., Williamson,
A., . . . Acker, J. D. (2005). Regional brain changes in aging healthy adults:
general trends, individual differences and modifiers. Cereb Cortex, 15(11), 1676-
1689. doi: 10.1093/cercor/bhi044
Rissman, J., Gazzaley, A., & D'Esposito, M. (2004). Measuring functional connectivity
during distinct stages of a cognitive task. Neuroimage, 23(2), 752-763. doi:
10.1016/j.neuroimage.2004.06.035
Rolls, E. T., & Grabenhorst, F. (2008). The orbitofrontal cortex and beyond: From affect
to decision-making. Progress in Neurobiology, 86, 216–244. doi:
10.1016/j.pneurobio.2008.09.001
Rosler, A., Ulrich, C., Billino, J., Sterzer, P., Weidauer, S., Bernhardt, T., . . .
Kleinschmidt, A. (2005). Effects of arousing emotional scenes on the distribution
of visuospatial attention: changes with aging and early subcortical vascular
dementia. J Neurol Sci, 229-230, 109-116. doi: 10.1016/j.jns.2004.11.007
Roudier, M., Marcie, P., Grancher, A. S., Tzortzis, C., Starkstein, S., & Boller, F. (1998).
Discrimination of facial identity and of emotions in Alzheimer's disease. J Neurol
Sci, 154(2), 151-158.
Ryan, J. D., & Cohen, N. J. (2004). Processing and short-term retention of relational
information in amnesia. Neuropsychologia, 42(4), 497-511.
107

Sakaki, M., Niki, K., & Mather, M. (2011). Updating existing emotional memories
involves the frontopolar/orbito-frontal cortex in ways that acquiring new
emotional memories does not. J Cogn Neurosci, 23(11), 3498-3514. doi:
10.1162/jocn_a_00057
Salat, D. H., Kaye, J. A., & Janowsky, J. S. (2001). Selective preservation and
degeneration within the prefrontal cortex in aging and Alzheimer disease. Arch
Neurol, 58(9), 1403-1408.
Satler, C., Garrido, L. M., Sarmiento, E. P., Leme, S., Conde, C., & Tomaz, C. (2007).
Emotional arousal enhances declarative memory in patients with Alzheimer's
disease. Acta Neurol Scand, 116(6), 355-360. doi: 10.1111/j.1600-
0404.2007.00897.x
Schoenbaum, G., Saddoris, M. P., & Stalnaker, T. A. (2007). Reconciling the roles of
orbitofrontal cortex in reversal learning and the encoding of outcome expectancies.
Ann N Y Acad Sci, 1121, 320-335. doi: 10.1196/annals.1401.001
Shattuck, D. W., Mirza, M., Adisetiyo, V., Hojatkashani, C., Salamon, G., Narr, K. L., . . .
Toga, A. W. (2008). Construction of a 3D probabilistic atlas of human cortical
structures. Neuroimage, 39(3), 1064-1080. doi:
10.1016/j.neuroimage.2007.09.031
Stalnaker, T. A., Franz, T. M., Singh, T., & Schoenbaum, G. (2007). Basolateral
amygdala lesions abolish orbitofrontal-dependent reversal impairments. Neuron,
54(1), 51-58. doi: 10.1016/j.neuron.2007.02.014
108

Swainson, R., Hodges, J. R., Galton, C. J., Semple, J., Michael, A., Dunn, B. D., . . .
Sahakian, B. J. (2001). Early detection and differential diagnosis of Alzheimer's
disease and depression with neuropsychological tasks. Dement Geriatr Cogn
Disord, 12(4), 265-280.
Thomas, R. C., & Hasher, L. (2006). The influence of emotional valence on age
differences in early processing and memory. Psychol Aging, 21(4), 821-825. doi:
10.1037/0882-7974.21.4.821
Tisserand, D. J., Pruessner, J. C., Sanz Arigita, E. J., van Boxtel, M. P., Evans, A. C.,
Jolles, J., & Uylings, H. B. (2002). Regional frontal cortical volumes decrease
differentially in aging: an MRI study to compare volumetric approaches and
voxel-based morphometry. Neuroimage, 17(2), 657-669.
Tomaszczyk, J. C., Fernandes, M. A., & MacLeod, C. M. (2008). Personal relevance
modulates the positivity bias in recall of emotional pictures in older adults.
Psychon Bull Rev, 15(1), 191-196.
Tomaszewski Farias, S., Cahn-Weiner, D. A., Harvey, D. J., Reed, B. R., Mungas, D.,
Kramer, J. H., & Chui, H. (2009). Longitudinal changes in memory and executive
functioning are associated with longitudinal change in instrumental activities of
daily living in older adults. Clin Neuropsychol, 23(3), 446-461. doi:
10.1080/13854040802360558
Treisman, A. (1998). Feature binding, attention and object perception. Philos Trans R
Soc Lond B Biol Sci, 353(1373), 1295-1306. doi: 10.1098/rstb.1998.0284
109

Tsuchida, A., Doll, B. B., & Fellows, L. K. (2010). Beyond reversal: A critical role for
human orbitofrontal cortex in flexible learning from probabilistic feedback.
Journal of Neuroscience, 30, 16868–16875. doi: 10.1523/JNEUROSCI.1958-
10.2010
Vallesi, A., McIntosh, A. R., & Stuss, D. T. (2011). Overrecruitment in the aging brain as
a function of task demands: evidence for a compensatory view. J Cogn Neurosci,
23(4), 801-815. doi: 10.1162/jocn.2010.21490
Weiler, J. A., Bellebaum, C., & Daum, I. (2008). Aging affects acquisition and reversal
of reward-based associative learning. Learn Mem, 15(4), 190-197. doi:
10.1101/lm.890408
Worsley, K. J. (2001). Statistical analysis of activation images. In P. Jezzard, P. M.
Matthews, & S. M. Smith (Eds.), Functional MRI: An introduction to methods.
New York: Oxford University Press, pp. 251–270.
Wright, C. I., Negreira, A., Gold, A. L., Britton, J. C., Williams, D., & Barrett, L. F.
(2008). Neural correlates of novelty and face-age effects in young and elderly
adults. Neuroimage, 42(2), 956-968. doi: 10.1016/j.neuroimage.2008.05.015
Yang, S. X., Kummar, S., Steinberg, S. M., Murgo, A. J., Gutierrez, M., Rubinstein,
L., . . . National Cancer Institute Phase 0 Working, Group. (2009).
Immunohistochemical detection of poly(ADP-ribose) polymerase inhibition by
ABT-888 in patients with refractory solid tumors and lymphomas. Cancer Biol
Ther, 8(21), 2004-2009.

Abstract (if available)

Abstract Older adults commonly experience difficulty remembering associative information. This can lead to a number of negative health outcomes and affects their quality of life. Thus, it is important to try to reduce the impact of the decline by understanding what factors might influence their memory performance. Given that emotional processing is well preserved in normal aging, it is possible that emotion modulates associative memory in a similar way in younger and older adults. The current study investigated this possibility by using behavioral and functional MRI (fMRI) methods. The behavioral results revealed that emotional arousal enhances or impairs associative memory depending on novelty of the items in both younger and older adults. The fMRI results suggested that both age groups showed similar patterns of activation in the amygdala and the frontopolar OFC regions. However, age-group differences were found when associative learning does not involve emotion

Linked assets

University of Southern California Dissertations and Theses

Conceptually similar

PDF

The impact of emotion, valence, and arousal on differential memory processes in younger and older people

PDF

Mechanisms of stress effects on learning and decision making in younger and older adults

PDF

Emotion, attention and cognitive aging: the effects of emotional arousal on subsequent visual processing

PDF

Emotional reactivity and memory biases in older and younger adults

PDF

Dedifferentiation of emotion regulation strategies in the aging brain: an MVPA investigation

PDF

Structure and function of the locus coeruleus across the lifespan

PDF

Reacting to the negative consequences of your decisions: an ATSS comparison of cognitive and affective reactions in older versus younger adults

PDF

Age differences in jealousy: an ATSS examination of the role of attributions in the emotional reactions of older and younger adults in relationship-threatening situations

PDF

Influence of age and anxiety on recognition of facial expressions of emotion: exploring the role of attentional processes

PDF

Aging and emotion regulation in the judgment of facial emotion

PDF

Noradrenergic mechanisms of arousal-enhanced memory selectivity

PDF

How age-related changes in the locus coeruleus affect selective attention and memory

PDF

The role of age, mood, and time- perspective on the interpretation of emotionally ambiguous information

PDF

Optimism when imagining the future in old age influences the positivity effect in memory

PDF

Value-based decision-making in complex choice: brain regions involved and implications of age

PDF

Statistical algorithms for examining gene and environmental influences on human aging

PDF

Using mixed methods to identify the characteristics of older fraud victims

PDF

Effects of estradiol on cortisol response, working memory, and emotional memory during stress in young and post-menopausal women

PDF

International sex and age differences in physical function and disability

PDF

Age differences in diffusivity in the locus coeruleus and its ascending noradrenergic tract

Asset Metadata

Creator Nashiro, Kaoru (author)

Core Title How emotional arousal influences memory and learning in younger and older adults

School Leonard Davis School of Gerontology

Degree Doctor of Philosophy

Degree Program Gerontology

Publication Date 07/23/2012

Defense Date 06/06/2012

Publisher University of Southern California (original), University of Southern California. Libraries (digital)

Tag aging,amygdala,arousal,associative memory,emotion,frontal pole,functional MRI,memory binding,memory updating,OAI-PMH Harvest,orbitofrontal cortex,parietal cortex,reversal learning

Language English

Contributor Electronically uploaded by the author (provenance)

Advisor Mather, Mara (committee chair), Davison, Gerald C. (committee member), Gatz, Margaret (committee member)

Creator Email kaoru28@hotmail.com,nashiro@usc.edu

Permanent Link (DOI) https://doi.org/10.25549/usctheses-c3-61195

Unique identifier UC11289467

Identifier usctheses-c3-61195 (legacy record id)

Legacy Identifier etd-NashiroKao-967.pdf

Dmrecord 61195

Document Type Dissertation

Rights Nashiro, Kaoru

Type texts

Source University of Southern California (contributing entity), University of Southern California Dissertations and Theses (collection)

Access Conditions The author retains rights to his/her dissertation, thesis or other graduate work according to U.S. copyright law. Electronic access is being provided by the USC Libraries in agreement with the a...

Repository Name University of Southern California Digital Library

Repository Location USC Digital Library, University of Southern California, University Park Campus MC 2810, 3434 South Grand Avenue, 2nd Floor, Los Angeles, California 90089-2810, USA