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Behavioural Science Section / Viewpoint
Gerontology 2012;58:156–163
DOI: 10.1159/000328465
Age Differences in Brain Activity during Emotion
Processing: Reflections of Age-Related Decline or
Increased Emotion Regulation?
Kaoru Nashiro Michiko Sakaki Mara Mather
Davis School of Gerontology, University of Southern California, Los Angeles, Calif. , USA
cortex activity than younger adults while engaging in emo-
tion-processing tasks, we argue that the cognitive control
hypothesis is a more likely explanation for older adults’ pos-
itivity effect than the aging-brain model.
Copyr ight © 2011 S. K arger AG, Basel
In contrast with the age-related declines in many do-
mains of cognitive functioning
[1] , emotion regulation
functioning improves somewhat with age
[2] . People ex-
perience less negative affect as they get older and can re-
store their good mood after being induced into a negative
mood more effectively than younger adults
[3] . Older
adults also show a ‘positivity effect’ in attention and
memory
[4] . For instance, older adults sometimes spend
a larger proportion of time viewing positive items and a
smaller proportion viewing negative items than do
younger adults
[5, 6] . Moreover, in some studies, com-
pared with younger adults, less of what older adults re-
member is negative and more is positive
[5, 7, 8] . Such age
by valence interactions tend to have a medium effect size
[8] ; thus, as might be expected, studies with relatively
small participant groups do not always reveal significant
age differences. Other factors, such as a level of arousal of
stimuli
[9] , availability of cognitive resources [6] or types
of mea surement s acro ss studies
[10] , may also account for
the presence or absence of a positivity effect.
Why do older adults show some improvements in
emotion regulation despite suffering age-related cogni-
Key Words
Emotion ⴢ Aging ⴢ Functional magnetic resonance
imaging ⴢ Positivity effect ⴢ Amygdala ⴢ Prefrontal cortex
Abstract
Despite the fact that physical health and cognitive abilities
decline with aging, the ability to regulate emotion remains
stable and in some aspects improves across the adult life
span. Older adults also show a positivity effect in their atten-
tion and memory, with diminished processing of negative
stimuli relative to positive stimuli compared with younger
adults. The current paper reviews functional magnetic reso-
nance imaging studies investigating age-related differences
in emotional processing and discusses how this evidence re-
lates to two opposing theoretical accounts of older adults’
positivity effect. The aging-brain model [Cacioppo et al. in:
Social Neuroscience: Toward Understanding the Underpin-
nings of the Social Mind. New York, Oxford University Press,
2011] proposes that older adults’ positivity effect is a conse-
quence of age-related decline in the amygdala, whereas the
cognitive control hypothesis [Kryla-Lighthall and Mather in:
Handbook of Theories of Aging, ed 2. New York, Springer,
2009; Mather and Carstensen: Trends Cogn Sci 2005;
9: 496–
502; Mather and Knight: Psychol Aging 2005; 20: 554–570] ar-
gues that the positivity effec t is a result of older adults’ great-
er focus on regulating emotion. Based on evidence for struc-
tural and functional preservation of the amygdala in older
adults and findings that older adults show greater prefrontal
Recei ved: January 11, 2011
Accepted: April 11, 2011
Publish ed online: June 21, 2011
Kaoru Na shiro
Davis School of Gerontology, Universit y of Southern Cal ifornia
3715 McCli ntock Avenue
Los A ngeles, CA 90089-0191 (USA)
Tel. +1 213 740 9401, E-Mai l nashiro
@ usc.edu
© 2011 S. Karger AG, Basel
0304–324X/12/0582–0156$38.0 0/0
Accessible online at:
www.karger.com/ger
Age Differences in Brain Activity during
Emotion Processing
Gerontology 2012;58:156–163
157
tive decline? One possibility is that age-related decline in
brain regions that monitor negative, potentially threaten-
ing information reduces negative affect. This is the argu-
ment made by Cacioppo et al.
[11] with their aging-brain
model which proposes that age-related decline in the
amygdala leads to the positivity effect. This argument is
based on the observation that patients with amygdala le-
sions are worse at rating the arousal or intensity of nega-
tive stimuli, but not of positive stimuli
[12, 13] . Cacioppo
et al.
[11] propose that age-related decline in the amyg-
dala selectively diminishes emotional arousal in response
to negative stimuli (but not positive stimuli) and, as a re-
sult, older adults fail to get the memorial advantage of
high arousal associated with negative stimuli and experi-
ence less negative affect.
A different possibility is that age-related diminish-
ment of negative affect occurs because older adults are
more focused on regulating emotion in their everyday
lives. Previous research suggests that older adults are
more likely than younger adults to prioritize emotion
regulatory goals over other goals
[14] , and to regulate
emotion when induced into a negative mood
[15] . Effec-
tive emotion regulation requires self-directed attention
and memory. For instance, attention should avoid nega-
tive information that could impair one’s mood and mem-
ory processes should be directed to increase the preva-
lence of positive mood-enhancing thoughts. Being guid-
ed by emotion regulation goals rather than by currently
salient stimuli requires the types of cognitive control pro-
cesses implemented by the prefrontal cortex (PFC)
[16] .
Based on this line of reasoning, the cognitive control
model
[3, 4, 7] argues that older adults’ positivity effect is
due to their greater focus on regulating emotions and re-
quires cognitive control processes. This idea is consistent
with behavioral evidence suggesting that the positivity
effect emerges especially when older adults have enough
cognitive resources, and when this effort is not readily
available, they show no positivity effect
[6, 17, 18] . Fur-
thermore, the positivity ef fect is most robust for items low
in a rous al , a s low ar ousi ng item s a re mor e l ik el y to engag e
cognitive control processes whereas high arousing items
require relatively automatic processes
[9] .
In this paper, we review recent functional magnetic
resonance imaging (f MRI) studies of age differences in
emotional processing and discuss how they relate to these
two opposing theoretical accounts of older adults’ posi-
tivity effect. The aging-brain and cognitive-control mod-
els make different predictions about how aging should
affect brain activity during emotion processing. The ag-
ing-brain model argues that age-related functional de-
cline in the amygdala causes the positivity effect, where-
as the cognitive control model assumes that prefrontal
regulation of emotional processing causes the positivity
effect.
Structural Preservation of the Amygdala in Aging
Imaging studies indicate that there is less volumetric
decline with age in the amygdala than in most other brain
regions
[19, 20] and postmortem measurements based on
histological staining reveal no significant effect of age on
amygdala volume
[21] . Thus, contrary to the aging-brain
model, older adults do not appear to suffer from focal
damage in the amygdala and patients with amygdala
damage are unlikely to be a useful neuropsychological
model of the effects of aging.
Consistent with the structural preservation of the
amygdala, emotional processing is well preserved in nor-
mal aging. Previous research suggests that the ability to
detect emotionally arousing stimuli is relatively stable
with age
[22] , and that the effects of emotional arousal on
memory remain intact in normal aging
[23] . Further-
more, younger and older adults produce similar skin con-
ductance responses to emotionally arousing stimuli
[23,
24] .
Functional Neuroimaging Comparisons of Younger
and Older Adults’ Amygdala Activity
Despite structural preservation of the amygdala in nor-
mal aging, fMRI studies have revealed some age differ-
ences in amygdala activity. The difference seen most con-
sistently across studies is an age-related decrease in activa-
tion i n response to negative sti mul i
[25–28] . This decrease
in amygda la ac tivity in res pon se to n ega tive s ti mul i is pre-
dicted by both theoretical perspectives. The aging-brain
model predicts that age-related amygdala decline reduces
amygda la responsivity to emotionally arousing stimuli. In
contrast, the cognitive-control model predicts that pre-
frontal emotion regulation processes diminish amygdala
responses to negative but not positive stimuli. Therefore,
age-related decreases in amygdala activity when viewing
negative stimuli are not due to inherent amygdala impair-
ments. Although both explanations are plausible, prior
studies provide more evidence for the cognitive control
model. Below, we first describe results consistent with the
cognitive control model, followed by results contradicting
the aging-brain model’s assumptions.
Nashiro/Sakaki/Mather
Gerontology 2012;58:156–163
158
In line with the cognitive-control model, past studies
revealed a link between diminished amygdala activity to
negative stimuli and emotion regulation skills. In one
study of participants between 30 and 54 years of age, but
not younger adults, reduced amygdala activity to negative
stimuli was associated with a trait tendency to use an ef-
fective emotion regulation strategy (i.e. reappraisal)
[25] .
That is, higher reappraisal tendency predicted lower
amygdala activation while viewing negative stimuli than
during neutral ones. Furthermore, in another study, old-
er adults who showed a lower amygdala signal to negative
stimuli showed more effective regulation of diurnal cor-
tisol levels in the week following the scan
[29] . Although
these are correlational results, they suggest that older
adults’ reduced amygdala response to negative stimuli
does not reflect impaired amygdala function, but instead
emotion regulation efforts.
Furthermore, research on Alzheimer’s disease (AD)
provides a counterpoint to the aging-brain model’s as-
sumption that decreased amygdala activity is a sign of
age-related decline in the amygdala. The amygdala is one
of the brain regions typically most affected by AD
[30] . A
study comparing amygdala responses in younger, older,
and AD patients while viewing familiar neutral and nov-
el fearfu l human faces revea led that the AD g roup showed
significantly greater amygdala responses to both types of
faces relative to elderly controls
[31] . Importantly, greater
hyperactivity was associated with greater severity of ir-
ritability and agitation symptoms in AD. The results sug-
gest that disease-related amygdala decline leads to hyper-
a ct i ve a m yg d al a re s po n se s . Th e re fo r e, t h is r ed uc e d am y g-
dala response to negative stimuli seen among healthy
older adults is not a symptom of early AD.
In addition, contrary to the aging-brain model’s as-
sumption that the amygdala declines with age, there is
evidence that the amygdala’s function is preserved in
healthy older adults
[32] . First, in two studies that includ-
ed both positive and negative pictures, age-related de-
creases in amygdala activity were seen for negative but
not positive pictures
[25, 26] . Thus, even in older adults
who showed reduced amygdala activity to negative stim-
uli, their amygdala can still be activated by a certain type
of emotional stimuli. Second, the amygdala in older
adults is sometimes activated even by negative stimuli. In
one study
[33] , for example, both younger and older adults
showed enhanced amygdala activity to negative photo-
graphs compared to neutral photographs. Importantly,
the amygdala activation in older adults involved overlap-
ping areas with younger adults, suggesting that older
adults depend on the same amygdala regions to process
negative stimuli as younger adults. Furthermore, re-
search on emotional memory demonstrated that the
amygdala plays an important role in enhancing memory
for emotional stimuli both in younger and older adults
[34 –36] . Taken together, these findings suggest that the
amygdala functions similarly in healthy older adults as it
does in younger adults. Thus, it seems unlikely that the
reduced amygdala activity to negative stimuli in older
adults is caused by age-related impairment of the amyg-
dala as the aging-brain model predicts.
Age-Related Differences in PFC Activity during
Emotion Processing
While the cognitive-control and aging-brain models
both predict reduced amygdala activity to negative stim-
uli in older adults, the two models make different predic-
tions about PFC activity during emotion processing. In
contrast to the aging-brain model, which makes no spe-
cific predictions about PFC responsivity to emotional
stimuli, the cognitive control model argues that if older
adults’ positivity effects are the result of a greater focus
on emotion regulation goals, older adults should recruit
more PFC while encountering emotional stimuli than do
younger adults because the PFC is involved in cognitive
control of emotion
[16, 29, 37] . Importantly, such age-re-
lated increases in PFC activity should exceed those seen
in response to neutral stimuli. Increases in PFC activity
are expected for downregulation of negative emotion (i.e.
dampening of emotional responses or attentional avoid-
ance of negative stimuli) and for upregulation of positive
emotion (i.e. enhancing emotional responses to positive
stimuli). To address these predictions, we review prior
studies examining age differences in PFC activity in re-
sponse to negative and positive stimuli (although there
are fewer studies with positive stimuli; further investiga-
tion is needed).
Greater PFC Activity to Negative Stimuli in Older
Adults
Consistent with the prediction made by the cognitive
control model, a number of studies report that older
adults recruited PFC more for negative than for neutral
stimuli compared with younger adults ( fig.1 ; table1 ). In
one study
[38] , brain activity was measured by fMRI
while younger and older adults made indoor-outdoor
judgments (i.e. encoding session) and old-new recogni-
Age Differences in Brain Activity during
Emotion Processing
Gerontology 2012;58:156–163
159
tion judgments about negative or neutral photographs
(i.e. recognition session). The results indicated that older
adults recruited dorsolateral PFC more strongly for nega-
tive photographs (than for neutral ones) compared with
younger adults in the encoding session. Similar patterns
were observed in the recognition session; older adults
showed increased dorsolateral PFC activity to negative
pictures together with reduced amygdala activity com-
pared with younger adults. Other studies also reveal that
older adults show increased PFC or anterior cingulate
cortex (ACC) activity together with decreased amygdala
activity while viewing negative stimuli
[27, 28] . In addi-
tion, relative to younger adults, older adults showed more
negative functional connectivity between the right amyg-
dala and ACC while rating emotional pictures
[33] . More-
over, the negative correlation between these two regions
was observed when older adults rated negative pictures as
neutral, but not when they rated negative pictures as neg-
ative. These results are consistent with the cognitive con-
trol model, suggesting that PFC/ACC dampened activity
in the amygdala while viewing negative stimuli, and that
the enhanced PFC activity seen in older adults reflects
their efforts to downregulate negative emotions.
Indeed, the PFC regions activated by older adults in
these studies (and in others; see table1 ) are similar to re-
gions implicated in emotion regulation. For instance,
Brodmann area (BA) 9 was also activated while people
we re told to down re gu la te th ei r negat ive e mot io ns to aver-
sive stimuli
[37, 39] . Likewise, BA 6, 8, 10, 44, and 45 over-
lap with areas associ ated with downregu lat ion of ne gative
emotion
[37] . While most emotion regulation findings are
based on younger adults, a recent study found that cogni-
tive reappraisal activated similar PFC regions to those
mentioned above in both younger and older adults
[40] .
In addition, there is evidence of negative relationships be-
tween the amygdala and PFC during successful emotion
regulation
[41, 42] , which is also consistent with the nega-
tive amygdala-PFC correlations seen in older adults when
they encounter negative stimuli
[33] . Taken together, these
studies suggest that the enhanced PFC activity to negative
stimuli coupled with decreased amygdala activity while
encountering negative stimuli may reflect older adults’ at-
tempts to regulate their emotions.
Greater PFC Activity to Positive versus Negative
Stimuli in Older Adults
In addition to increased PFC when processing nega-
tive stimuli, older adults sometimes recruit PFC more for
positive than negative stimuli (relative to younger adults;
see table2 and fig.2 ). Older adults’ increased PFC activ-
ity to positive stimuli has been observed when a task re-
quires more elaborative processing of emotional stimuli,
rather than passive viewing (such as self-relevant process-
ing
[43] , semantic judgments [44] , or mental manipula-
tion of the perceptual stimulus representation
[45] ). This
may suggest that, when prompted to deeply process stim-
uli, older adults engage more with positive than negative
stimuli. This idea is supported by two studies examining
how the depth of encoding affects brain activit y in young-
er and older adults.
In Ritchey et al. [44] , younger and older adults viewed
positive, negative, or neutral photographs, and either
analyzed each picture for its semantic meanings (i.e. se-
mantic elaboration condition), or focused on the colors
and lines in the pictures (i.e. shallow condition). In old-
er adults, positive stimuli induced greater activity in
medial/superior PFC and inferior PFC under the se-
mantic elaboration condition, but not under the shallow
Fig. 1. Age differences in PFC involvement while processing neg-
ative stimuli. Negative stimuli induced greater PFC activity com-
pared with neutral stimuli in older adults compared to younger
adults (represented by black dots; online version: red dots). In
some studies, where participants could anticipate negative stim-
uli, older adults showed less PFC activity than did younger adults
(represented by white dots; online version: blue dots). See table1
for a list of coordinates and studies used in the figure.
Color versi on available online
Nashiro/Sakaki/Mather
Gerontology 2012;58:156–163
160
condition. In contrast, in younger adults, these PFC
clusters showed similar levels of activity to positive
stimuli regardless of the condition. Similar results were
observed in another study
[43] ; compared with younger
adults, older adults recruited medial and middle PFC
more for positive items relative to negative items when
they made self-referential judgments about those stim-
uli (relative to other-referential judgments). Both se-
mantic elaboration and self-referential processing are
known to induce deep processing, requiring cognitive
effort
[46] . Thus, it appears that older adults recruit PFC
for positive stimuli especially when they process those
stimuli deeply.
According to the cognitive control model, older adults’
greater PFC activity for positive stimuli described above
is a result of their effort to upregulate emotion to experi-
ence more positive affect. If this is the case, older adults’
brain regions activated while processing positive stimuli
should a lso activ ate when pe ople upregulate or t ry to a m-
plify their positive emotions. Although most emotion
regulation studies have focused on downregulation of
negative affect, one study
[47] used positive and negative
stimuli in order to identify regions critical for upregula-
tion of positive emotions. The identified regions included
the dorsomedial PFC (BA 6), the left PFC (BA 8), the me-
dial PFC (BA 10), the medial orbitofrontal cortex (BA 11),
and left orbitofrontal cortex (BA 47). Importantly, these
Tab le 1. Summary of neuroimaging studies showing age-related differences in prefrontal cortex activity to negative vs. neutral stimuli
Study Stimulus Task Contrast Age effects BA x y z
Roalf et al. [49] IAPS pictures (positive,
negative, or neutral)
passively viewing [negative > neutral] OA > YA –34 14 32
Williams et al. [48] faces passively viewing [negative > neutral] OA > YA 8 –18 25 42
(fear, happy, or neutral) OA > YA 8 6 40 44
Murty et al. [38] IAPS pictures (negative or
neutral)
indoor-outdoor judgment [negative > neutral] OA > YA 10 –26 50 15
IAPS pictures (negative or
neutral)
recognition task [negative > neutral] OA > YA 46 44 24 25
IAPS pictures (negative or
neutral)
recognition task [negative > neutral] OA > YA 24 6 4 36
Tessitore et al. [27] faces (fear or angry) or facial expression matching [negative-neutral] OA > YA 9 –36 15 22
geometric shapes task or sensorimotor task OA > YA 44/45 32 15 22
OA > YA 8 –10 31 40
St. Jacques et al. [34] IAPS pictures (negative or
neutral)
valence rating [negative R-negative F] >
[neutral R-neutral F]
OA > YA 9 –43 27 36
St. Jacques et al. [33] IAPS pictures valence rating [negative > neutral] OA > YA 6 33 0 57
(negative or neutral) OA > YA 9 2 28 39
Fischer et al. [35] faces (fearful or neutral) fear or neutral judgment [negative R-negative F] >
[neutral R-neutral F]
OA > YA 9 23 36 35
Erk et al. [25] cues predicting IAPS
pictures (negative, positive,
or neutral)
anticipating a picture
corresponding to the
valence of the cue
[negative > neutral] YA > OA 32 –4 42 0
IAPS pictures (positive,
negative or neutral)
passively viewing [negative > neutral] YA > OA 46 52 22 20
Williams et al. [48] faces passively viewing [negative > neutral] YA > OA 8 –18 25 42
(fear, happy, or neutral) YA > OA 8 6 40 44
St. Jacques et al. [34] IAPS pictures valence rating [negative R-negative F] > YA > OA 6 –26 –6 44
(negative or neutral) [neutral R-neutral F] YA > OA 9 –15 31 30
YA > OA 6 9 16 52
YA > OA 6 12 –11 57
R = Remembered; F = forgotten; YA = younger adults; OA = older adults; BA = Brodmann area. Coordinates are in MNI space and plotted in figure 1.
Age Differences in Brain Activity during
Emotion Processing
Gerontology 2012;58:156–163
161
regions were similar to those activated more for positive
than negative stimuli while older adults were deeply en-
gaged with these stimuli (BA 8, 10, 11, and 47 shown in
table2 ). This provides further support for the cognitive
co ntrol model, sug gest ing t hat olde r adu lts tend to re cr ui t
PFC when encountering positive stimuli in order to feel
more positive.
Questions for Future Research
While many studies have reported enhanced PFC ac-
tivity to emotional stimuli in older in comparison to
younger adults (as reviewed above), a few studies have
reported decreased PFC activity to positive stimuli
[25,
48] and negative stimuli in older adults compared to
younger adults
[25, 49] . Some of these age-related reduc-
tions in PFC activity during emotion processing may be
related to the stimuli presentation sequences used. For
instance, in one such study
[25] , participants were given
symbolic cues that informed them about the valence of
the subsequent picture. Being able to anticipate negative
emotional stimuli may have allowed older adults to en-
gage in antecedent-focused regulation (strategies to reg-
ulate emotion before the emotional response has already
been fully activated
[50] ) rather than response-focused
regulation that requires more cognitive control. In an-
other study
[49] , participants viewed blocks of 40 pic-
tures of the same valence for 80 s. Overall, older adults
had reduced amygdala activity compared with younger
adults, especially while viewing the negative pictures.
Older adults a lso showed more PFC activit y than young-
er adults during the first 20 negative pictures, but this
greater prefrontal activity habituated by the second half
of the blocks. Younger adults did not show this pattern
of habituation for any emotional valence and older adults
only showed it for the negative pictures. It is possible that,
during the 80-second long blocks of negative pictures,
older participants initially had emotional responses to
each picture and then attempted to downregulate these
emotional responses. As the series of negative pictures
continued, however, they may have switched to less tax-
ing antecedent-focused strategies in which they attempt-
ed to avoid having a response to the pictures in the first
place. Further research is needed to investigate the role
of anticipation of negative affect and how it might affect
older adults’ PFC engagement while processing negative
stimuli.
Summary and Future Directions
This paper compares two theoretical accounts for old-
er adults’ positivity effect. The aging-brain model pro-
poses that age-related decline in amygdala activation in
response to negative stimuli causes an age-related posi-
tivity bias in cognition. In contrast, the cognitive control
model argues that older adults’ motivational changes di-
rect cognitive control processes to regulate emotion,
leading to a positivity effect. Arguing against the aging-
brain model, previous neuroimaging evidence suggests
that the amygdala remains structurally intact and func-
tionally responsive to various types of stimuli including
negatively valenced items. Furthermore, although par-
ticipants were not instructed to regulate negative or pos-
itive emotions explicitly in most studies cited in this pa-
per, older adults showed enhanced PFC activity during
emotion processing tasks (relative to neutral conditions)
compared with younger adults. These observations are
Color versi on available online
Fig. 2. Age differences in PFC involvement while processing pos-
itive stimuli. Although some studies showed greater PFC activity
to positive stimuli than to neutral stimuli in younger adults than
in older adu lts (shown by wh ite dots; online version: blue dots), in
studies with tasks requiring deep processing of stimuli, older
adults recruited PFC more for positive stimuli than for negative
stimuli (relative to younger adults), which is shown by black dots
(online version: red dots). See table2 for a list of coordinates and
studies used in the figure.
Nashiro/Sakaki/Mather
Gerontology 2012;58:156–163
162
consistent with the possibility that emotion regulation
goals are more chronically active for older adults than for
younger adults
[4, 7] . This idea is further supported by the
overlap in brain regions activated during emotion pro-
cessing (with no instructions to regulate emotions in-
duced by emotional stimuli) and during emotion regula-
tion (with specific instructions to regulate emotion).
Future research should investigate age differences in
brain activity during spontaneous versus strategic emo-
tion regulation (especially upregulation of positive emo-
tion, which has not been well investigated). This would
elucidate how much of older adults’ emotion regulation
mechanism is chronically activated and how much of it is
intentional, and how these underlying mechanisms affect
their mood and cognition in general.
Acknowledgements
This work was supported by grants f rom the National Institute
on Aging (R01AG025340, R01AG038043, K02AG032309 and
5T32AG000037). We would also like to acknowledge Lin Nga for
assisting with the figures.
Tab le 2. Summary of neuroimaging studies showing age-related differences in prefrontal cortex activity to positive vs. negative or
neutral stimuli
Study Stimulus Task Contrast Age effects BA x y z
Addis et al. [45] photo objects (positive, size judgments [positive > negative] OA > YA 10/32 –1 35 3
negative, or neutral) OA > YA 10/11/47 –34 40 0
Kensinger and photo objects (positive, size judgments during [positive R > positive F]- OA > YA 10 –1 30 –2
Schacter [36] negative, or neutral) encoding and [negative or neutral R > OA > YA 24 –8 22 15
recognition test negative or neutral F] OA > YA 33 8 6 28
Leclerc and photo objects (positive, size judgments [positive > negative] OA > YA 8 –36 24 48
Kensinger [22] negative, or neutral) OA > YA 32 0 40 –4
OA > YA 32 12 48 8
Ritchey et al. [44] IAPS pictures semantic elaboration age X task X valence masked OA > YA 32 17 32 18
(positive, negative, or color processing with [positive > negative in OA] OA > YA 10 –8 38 19
or neutral) X [deep > shallow in OA] OA > YA 10 –22 49 9
OA > YA 10 20 49 4
OA > YA 45 –39 15 14
Gutchess et al. [43] positive and negative self, other (Einstein) [self positive-other positive] > OA > YA 8 –28 12 54
adjectives or case judgments [self negative-other negative] OA > YA 45 50 46 6
OA > YA 32 12 38 40
Erk et al. [25] IAPS pictures (positive,
negative, or neutral)
passively viewing [positive > neutral] YA > OA 9 –2 64 20
Williams et al. [48] faces (fear, happy, neutral) passively viewing [positive > neutral] YA > OA 6 –18 22 54
YA > OA 10 20 54 –2
R = Remembered; F = forgotten; YA = younger adults; OA = older adults; BA = Brodmann area. Coordinates are in MNI space and plotted in figure 2.
References
1 Salthouse TA: Selective review of cognitive
aging. J Int Neuropsychol Soc 2010;
16: 754–
760.
2 Charles ST, Piazza JR: Age differences in a f-
fective well-being: context matters. Soc Per-
sonal Psychol Compass 2009;
3: 1–14.
3 Kryla-Lighthall N, Mather M: The role of
cognitive control in older adults’ emotional
well-being; in Berngtson V, Gans D, Putney
N, Silverste in M (eds): Handbook of Theorie s
of Aging, ed 2. New York, Springer Publish-
ing, 2009, pp 323–344.
4 Mather M, Carstensen LL: Aging and moti-
vated cog nition: the posit ivity effe ct in atten-
tion and memory. Trends Cogn Sci 2005;
9:
496–502.
5 Mather M, Carstensen LL: Aging and atten-
tional biases for emotional faces. Psychol Sci
2003;
14: 409.
6 Knight M, Seymour TL, Gaunt JT, Baker C,
Nesmith K, Mather M: Aging and goal-di-
rected emotional attention: distraction re-
verses emotional biases. Emotion 2007;
7:
705–714.
7 Mat her M, Knight M: Goal-directed memo-
ry: the role of cognitive control in older
adults’ emotional memory. Psychol Aging
2005;
20: 554–570.
8 Charles ST, Mather M , Carstensen LL : Aging
and emotional memory: the forget table na-
ture of negat ive images for older adult s. J Exp
Psychol Gen 2003;
132: 310 –324 .
9 Kensinger EA: Age differences in memory
for arousing and nonarousing emotional
words. J Gerontol B Psychol Sci Soc Sci 200 8;
63:P13–P18.
Age Differences in Brain Activity during
Emotion Processing
Gerontology 2012;58:156–163
163
10 Murphy NA, Isaac owitz DM: Preferences for
emotional i nformation in older and younger
adults: a met a-analysis of memor y and atten-
tion tasks. Psychol Aging 2008;
23: 263–286.
11 Cacioppo JT, Berntson GG, Bechara A, Tra-
nel D, Hawkley LC: Could an aging brain
contribute to subjective well-being? The val-
ue added by a social neuroscience perspec-
tive; in Todorov A, Fiske S, Prentice D (eds):
Social Neuroscience: Toward Understand-
ing the Underpinnings of the Social Mind.
New York, Oxford University Press, 2011,
p 249.
12 Bernts on GG, Bechara A , Damasio H, Tranel
D, Cacioppo JT: Amygdala contribution to
selective dimensions of emotion. Soc Cogn
Affect Neurosci 2007;
2: 123–129.
13 Adolphs R, Tranel D: Impai red judgments of
sadnes s but not happiness followi ng bilateral
amygda la damage. J Cog n Neurosci 200 4;
16:
453–462.
14 Carstensen LL, Isaacowitz DM, Charles ST:
Ta ki ng t im e s er iou s ly. A t he or y o f s oc io em o-
tional selectivity. Am Psychol 1999;
54: 165–
181.
15 Isaacowitz DM, Toner K, Goren D, Wilson
HR: Lo oking while un happy: mood-congr u-
ent gaze in you ng adults, posit ive gaze in old-
er adults. Psychol Sci 2008;
19: 848–853.
16 Ochsner KN, Gross JJ: The cognitive control
of emotion. Trends Cogn Sci 2005;
9: 242–
249.
17 Isaacowitz DM, Toner K , Neupert SD: Use of
gaze for rea l-time mood reg ulation: ef fects of
age and att entional func tioning. Psychol Ag-
ing 2009;
24: 989–994.
18 Petrican R, Moscovitch M, Schimmack U:
Cognitive resources, valence, and memory
retrieval of emotional events in older adults.
Psychol Aging 2008;
23: 585–594.
19 Mather M: Ag ing and emotional memor y; in
Reisberg D, Hertel P (eds): Memory and
Emotion. London, Oxford University Press,
2004, pp 272–307.
20 Allen JS, Bruss J, Brown CK, Damasio H:
Normal neuroanatomical variation due to
age: the major lobes and a parcellation of the
temporal region. Neurobiol Aging 2005;
26:
1245–1260.
21 B r ab e c J , R u l s e h A , H oy t B , V iz e k M , H o r i n ek
D, H or t J, P etr ov ick y P: Volu met ry of t he hu -
man amygdala – an anatomical study. Psy-
chiatr y Res 2010;
182: 67–72.
22 Leclerc CM, Kensinger EA: Effects of age on
detection of emotional information. Psychol
Aging 2008;
23: 209–215.
23 Denburg NL, Buchanan D, Tranel D,
Adolphs R: Evidence for preserved emotion-
al memory in normal elderly persons. Emo-
tion 2003;
3: 239–253.
24 Neiss MB, Leigla nd LA, Carlson NE,
Janowsky JS: Age differences in perception
and awareness of emotion. Neurobiol Aging
2009;
30: 1305–1313.
25 Erk S, Walter H, Abler B: Age-related physi-
ological responses to emotion anticipation
and exposure. Neuroreport 2008;
19: 447–
452.
26 Mather M, Canli T, English T, Whitfield SL,
Wais PE, Ochsner K N, John DEG, Ca rstensen
LL: Amygdala responses to emotionally va-
lenced stimuli in older and younger adults.
Psychol Sci 2004;
15: 259–263.
27 Tessitore A, Hariri AR, Fera F, Smith WG,
Das S, Weinberge r DR, Mattay VS: Func tion-
al cha nges in the act ivity of brai n regions un-
derlying emotion processing in the elderly.
Psychiatry Res 2005;
139: 9–18.
28 Fischer H, Sandblom J, Gavazzeni J, Frans-
son P, Wright CI, Backman L: Age-differen-
tial patterns of brain activation during per-
ception of angry faces. Neurosci Lett 2005;
386: 99–104.
29 Urry HL, va n Reekum CM, Johnstone T, Ka-
lin NH, Thurow ME, Schaefer HS, Jackson
CA, Frye CJ, Greischar LL, Alexander AL ,
Davidson RJ: Amygdala and ventromedial
prefrontal cortex are inversely coupled dur-
ing regulation of negative affect and predict
the diurnal pattern of cortisol secretion
among older adults. J Neurosci 20 06;
26:
4415–4425.
30 Liu Y, Paajanen T, Zhang Y, Westman E,
Wahlund LO, Simmons A, Tunnard C, So-
bow T, Mecocci P, Tsolaki M, Vellas B,
Muehlboeck S, Evans A, Spenger C, Love-
stone S, Soininen H: Analysis of regional
MRI volumes and thicknesses as predictors
of conversion from mild cognitive impair-
ment to Alzheimer’s disease. Neurobiol Ag-
ing 2010;
31: 1375–1385.
31 Wright CI, Dickerson BC, Feczko E, Negeira
A, Williams D: A functional magnetic reso-
nance imaging study of amygdala responses
to human faces in aging and mild Alzhei-
mer’s disease. Biol Psychiatry 2007;
62: 1388–
1395.
32 Wright CI, Negreira A, Gold AL, Britton JC,
Williams D, Feldman Barrett L: Neural cor-
relates of novelty and face-age effects in
young and elderly adults. Neuroimage 2008;
42: 956–968.
33 St. Jacques PL, Dolcos F, Cabeza R: Ef fects of
aging on f unctional connectivity of the
amygdala during negative evaluation: a net-
work analysis of fMRI data. Neurobiology
Aging 2010;
31: 315–327.
34 St. Jacques PL, Dolcos F, Cabeza R: Ef fects of
aging on f unctional connectivity of the
amygdala for subsequent memory of nega-
tive pictures. Psychol Sci 2009;
20: 74– 84.
35 Fischer H, Nyberg L, Backman L: Age-relat-
ed differences in brain regions supporting
successful encoding of emotional faces. Cor-
tex 2010;
46: 490–497.
36 Kensinger EA, Schacter DL: Neural process-
es supporting young and older adults’ emo-
tional memories. J Cogn Neurosci 2008;
20:
1161–1173.
37 Ochsner KN, Ray R D, Cooper JC, Robert son
ER, Chopra S, Gabrieli JDE, Gross JJ: For
better or for worse: neural systems support-
ing the cog nitive down- and up-re gulation of
negative emotion. Neuroimage 2004;
23:
483–499.
38 Murty VP, Sambataro F, Das S, Tan H-Y,
Callicott JH, Goldberg TE, Meyer-Linden-
berg A, Weinberger DR, Mattay VS: Age-re-
lated alterations in simple declarative mem-
ory and the effect of negative stimulus va-
lence. J Cogn Neurosci 2009;
21: 1920–1933.
39 van Reekum CM, Johnstone T, Urry HL,
Thurow ME, Schaefer HS, Alexander AL,
Davidson RJ: Gaze fixations predict brain
activation during the voluntary regulation of
picture-induced negative affect. Neuroim-
age 2007;
36: 1041–1055.
40 Winecoff A, Labar KS, Madden DJ, Cabeza
R, Huettel SA : Cognitive and ne ural contrib-
utors to emotion regulation in aging. Soc
Cogn Affect Neurosci 2011;
6: 165–176.
41 Urry HL, van Reekum CM, Joh nstone T, Da-
vidson RJ: Individual differences in some
(but not all) medial prefrontal regions reflect
cognitive demand while regulating unpleas-
ant emotion. Neuroimage 2009;
47: 852–863.
42 Wager TD, Davidson ML, Hughes BL,
Lindqui st MA, Ochsner KN: Pre frontal-sub-
cortic al pathways mediat ing successf ul emo-
tion regulation. Neuron 2008;
59: 1037–1050.
43 Gutchess AH, Kensinger EA, Schacter DL:
Aging, self-referencing, and medial prefron-
tal cortex. Soc Neurosci 2007;
2: 117.
44 Ritchey M, Bessette-Symons B, Hayes SM,
Cabeza R: Emotion processing in the aging
brain is modulated by semantic elaboration.
Neuropsychologia 2011;
49: 640–650.
45 Addis DR, Leclerc CM, Muscatell K, Ken-
singer EA: There are age-related changes in
neural connectivity during the encoding of
positive, but not negative, information. Cor-
tex 2009;
46: 425–433.
46 Glisky EL, Marquine MJ: Semantic and self-
referential processing of positive and nega-
tive trait adjectives in older adults. Memory
2009;
17: 144–157.
47 Kim SH, Hamann S: Neural correlates of
positive and negative emotion regulation. J
Cogn Neurosci 2007;
19: 776–798.
48 Williams LM, Brown KJ, Palmer D, Liddell
BJ, Kemp AH, Olivieri G, Peduto A, Gordon
E: Th e me ll ow y ea rs ? Ne ur al ba sis of imp ro v-
ing emotiona l stability over age. J Neurosci
2006;
26: 6422–6430.
49 Roalf DR, Pruis TA, Stevens AA, Janowsky
JS: More is less: emotion induced prefrontal
cortex activity habituates in aging. Neuro-
biol Aging 2009, E-pub ahead of print.
50 Gross JJ: Emotion regulation in adult hood:
timing is everyt hing. Curr Dir Psychol Sci
2001;
10: 214–219.