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Age Differences in Brain Activity during Emotion Processing: Reflections of Age-Related Decline or Increased Emotion Regulation?

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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 attention and memory, with diminished processing of negative stimuli relative to positive stimuli compared with younger adults. The current paper reviews functional magnetic resonance imaging studies investigating age-related differences in emotional processing and discusses how this evidence relates to two opposing theoretical accounts of older adults' positivity effect. The aging-brain model [Cacioppo et al. in: Social Neuroscience: Toward Understanding the Underpinnings of the Social Mind. New York, Oxford University Press, 2011] proposes that older adults' positivity effect is a consequence 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] argues that the positivity effect is a result of older adults' greater focus on regulating emotion. Based on evidence for structural and functional preservation of the amygdala in older adults and findings that older adults show greater prefrontal cortex activity than younger adults while engaging in emotion-processing tasks, we argue that the cognitive control hypothesis is a more likely explanation for older adults' positivity effect than the aging-brain model.
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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 Aging Functional magnetic resonance
imaging Positivity effect Amygdala 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 models 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 amygdalas 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 ; table1 ). 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 table1 ) 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 table2 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 table1
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
table2 ). 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 table2 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.
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... In general, older adults are thought to report higher levels of well-being (Charles et al., 2001;Scheibe and Carstensen, 2010) in part due to what has been described as a positivity effect whereby older adults attend to and remember positive information more than negative information compared to younger adults (Mather and Carstensen, 2005). This shift toward positive emotion may be a result of increased motivation to focus on emotional goals (e.g., maintaining social relationships; socioemotional selectivity theory, Carstensen et al., 1999), leading to an overall increase in the use of some ER skills with aging (Charles et al., 2009;Urry and Gross, 2010;Nashiro et al., 2012). Additionally, this positivity effect seems to be most prominent among older adults who are able to engage greater cognitive control (see review, Mather and Carstensen, 2005). ...
... Researchers have documented changes in brain activation, as measured by functional magnetic resonance imaging (fMRI), that may underlie older adults' ability to better utilize ER strategies while processing emotional stimuli. Findings demonstrate a decrease in amygdala activation to negative stimuli with age, a phenomenon that has been linked to ER skills (see review, Nashiro et al., 2012). Further, compared to younger adults, older adults exhibit greater prefrontal cortex (PFC, a region implicated in ER processes; Nashiro et al., 2012) activation while viewing emotionally salient stimuli, suggesting greater sponta neous engagement in ER strategies. ...
... Findings demonstrate a decrease in amygdala activation to negative stimuli with age, a phenomenon that has been linked to ER skills (see review, Nashiro et al., 2012). Further, compared to younger adults, older adults exhibit greater prefrontal cortex (PFC, a region implicated in ER processes; Nashiro et al., 2012) activation while viewing emotionally salient stimuli, suggesting greater sponta neous engagement in ER strategies. These findings support the conceptualization that adaptive changes in older adults are not due to age-related cognitive deficits, but rather a greater focus on ER goals (Nashiro et al., 2012;Kryla-Lighthall and Mather, 2009). ...
Article
Emotion regulation (ER) processes in older adults may be important for successful aging. Neural correlates of ER processes have been examined using event-related brain potentials (ERPs), such as the late-positive potential (LPP) during cognitive reappraisal paradigms. The current study sought to extend this research by examining the LPP from an ER task in a sample of 47 community-dwelling older adults between the ages of 60 and 84 years, scoring either high on emotional well-being (as measured by habitual ER use and resiliency; high WB group, n = 20) or low on emotional well-being (as measured by habitual ER use, resiliency, and depression; low WB group, n = 27). Participants viewed unpleasant and neutral images and were instructed to simply react to the images or reappraise their emotional response. Both pre- and post-instruction LPP amplitudes were scored, in addition to self-reported ratings of negative emotion collected during the task. We found greater LPP amplitude to emotionally salient compared to neutral stimuli, reduced LPP amplitude following instructions to reappraise emotional response to stimuli across groups, and a blunted LPP overall for individuals with higher depressive symptoms. Additionally, we demonstrated that older adults with low emotional well-being were less successful at reappraisal according to self-reported ratings of negative emotion, although this was not reflected in the LPP. Collectively, these data suggest that laboratory-based ER tasks might be used to understand abnormal ER use—though the LPP may be more sensitive to depression than individual differences in ER ability.
... Au niveau cérébral, les processus émotionnels impliqueraient un nombre important de régions cérébrales impliquées dans les processus perceptuels, moteurs, motivationnels et (Clarys et al., 2009;Hilgard et al., 2014;Salthouse, 1996Salthouse, , 2009, les capacités émotionnelles des personnes âgées ne semblent cependant pas suivre le même déclin. Il apparait, en effet, que les personnes âgées montrent une capacité soutenue, voire améliorée, en matière de régulation des émotions par rapport à des adultes plus jeunes (Sakaki et al., 2012). ...
... D'autre études ont établi un lien entre l'effet de positivité et une activation accrue du cortex préfrontal (Dolcos et al., 2014;Leclerc & Kensinger, 2011;Sakaki et al., 2012). Dans des tâches de mémoire ou de rappel autobiographique d'évènements négatifs, certains auteurs ont ainsi observé une augmentation de l'activité du cortex préfrontal ventro-médian (VmPFC) couplée à une diminution de l'activité de l'amygdale et une connectivité accrue entre le cortex préfrontal médian et l'amygdale chez les personnes âgées par rapport aux jeunes adultes (Sakaki et al., 2012)). ...
... D'autre études ont établi un lien entre l'effet de positivité et une activation accrue du cortex préfrontal (Dolcos et al., 2014;Leclerc & Kensinger, 2011;Sakaki et al., 2012). Dans des tâches de mémoire ou de rappel autobiographique d'évènements négatifs, certains auteurs ont ainsi observé une augmentation de l'activité du cortex préfrontal ventro-médian (VmPFC) couplée à une diminution de l'activité de l'amygdale et une connectivité accrue entre le cortex préfrontal médian et l'amygdale chez les personnes âgées par rapport aux jeunes adultes (Sakaki et al., 2012)). Il est connu que la régulation émotionnelle volontaire est associée à une diminution de l'activité de l'amygdale et une augmentation de celle du cortex préfrontal médian (Drabant et al., 2008). ...
Thesis
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La prévalence des stimuli négatifs classiquement observée chez de jeunes adultes s’atténue au cours du vieillissement sain, voire évolue vers une prévalence des stimuli positifs. Cet effet lié à l’âge est appelé « effet depositivité ». Présent dans des tâches d’évaluation du ressenti émotionnel, cet effet disparait lors de tâche d’évaluation de la tendance à l’action, suggérant une dissociation entre émotion et comportement d’action. Mieux comprendre l’évolution du lien entre processus émotionnels et comportements d’action au cours du vieillissement sain permettrait de préciser les conditions d’émergence de l’effet de positivité et de mieux comprendre les troubles moteurs et affectifs associés dans certaines pathologies neurodégénératives telles que la maladie de Parkinson. Le premier volet d’études de la thèse a consisté à évaluer l’évolution du traitement émotionnel au cours du vieillissement sain. Lors d’une tâche d’exploration libre de paires d’images émotionnelles, une première étude enoculométrie montre chez les personnes âgées une orientation automatique de l’attention réduite et une exploration attentionnelle plus focalisée spatialement pour les scènes positives, par rapport aux adultes jeunes et d’âge moyen.Au niveau cérébral, une seconde étude en IRM fonctionnelle (IRMf) suggère une réorganisation cérébrale au coursdu vieillissement sain qui traduirait une évolution des stratégies de traitement émotionnel : alors que les jeunes personnes activeraient plutôt un réseau fronto-limbique associé à l’évaluation et la régulation émotionnelles et à un traitement cognitif plus complexe, les personnes âgées (vs jeunes) activeraient davantage des régions liées à l’intégration viscéro-somato sensorielle, à la visualisation spatiale et à la programmation et régulation motrice dans une stratégie plus incarnée de l’évaluation émotionnelle. En revanche, les deux groupes, jeunes et âgés, se distinguent moins dans la tâche de tendance à l’action, suggérant des stratégies cérébrales de traitement émotionnel quasi-analogues pour décider d’une action motivée. Le deuxième volet d’études de la thèse a consisté à évaluer l’évolution du traitement émotionnel chez des patients parkinsoniens de novo en utilisant les mêmes protocoles des études précédentes. L’étude en oculométrie (3ème étude) révèle chez les patients, une orientation automatique de l’attention réduite pour les scènes émotionnelles (vs neutres) et d’autant plus pour les scènes positives et une exploration attentionnelle globalement plus étendue, par rapport aux contrôles sains. L’étude en IRMf (4ème étude)révèle, quant à elle, une suractivation d’un large réseau temporo-parieto-fronto-limbique spécifiquement dans latâche de tendance à l’action chez les patients (vs contrôles sains), suggérant un mécanisme de compensation aux difficultés rencontrées par les patients dans cette tâche, alors que leur évaluation émotionnelle est relativemen tpréservée. Les patterns oculomoteurs et cérébraux observés spécifiquement chez les patients parkinsoniens denovo ouvrent la piste à l’identification de potentiels nouveaux (bio)marqueurs précoces de la maladie de Parkinson et la tâche de tendance à l’action semble être un outil d’intérêt dans cette perspective.
... Authors interpret older adults' slower performance for probes replacing negative stimuli as a tendency to avoid negative instead of a preference for positive stimuli. Interestingly, this pattern emerges with longer cue presentation compared to shorter presentation, suggesting that the age-related bias in the negative condition is likely mediated by active control mechanisms [14,19,21]. However, these studies evaluated only the competition between an affective image (positive or negative) and a neutral one. ...
... These researchers found a negative bias in the negative-positive pair but only in younger participants. Moreover, as in previously mentioned studies [19,21], this pattern emerges only when the cue is presented for a sufficiently long interval, suggesting again a mediation of active top-down control mechanisms during affective information processing. Few studies have investigated short time intervals [20,22], and none of these has reported significant effects of implicit bottom-up affective information processing. ...
Article
Full-text available
Affective information is processed in different ways across one’s lifespan. Explanations for this pattern of performance are multiple and range from top-down motivational shifts and cognitive control to faster bottom-up and implicit processes. In this study, we aimed to investigate implicit affective information processing and positivity effects by examining performance in a modified version of the dot-probe task across three image-pair conditions (positive/neutral; negative/neutral; and positive/negative). We examined data from 50 older adults and 50 younger adults. The results showed that affective information processing varies with age and valence and that age effects in affective processing may occur early during information processing. Positivity biases emerge in both younger and older adults. However, while younger adults seem to prioritize positive information independently of context, older adults showed this prioritization only when presented in an emotional (i.e., negative) context. Moreover, older adults showed a tendency to avoid negative information whereas younger adults showed a general bias for affective content modulated by image-pair context.
... Past studies report relative preservation of both structure and function of the amygdala in normal aging (Good et al., 2001;Mather, 2016;Nashiro, Sakaki, & Mather, 2012). Alongside with this, emotional processing also appears to be spared in aging (Nashiro et al., 2012). ...
... Past studies report relative preservation of both structure and function of the amygdala in normal aging (Good et al., 2001;Mather, 2016;Nashiro, Sakaki, & Mather, 2012). Alongside with this, emotional processing also appears to be spared in aging (Nashiro et al., 2012). Our results align with these findings, since the amygdala maintains its importance in the brain structural network along time, both in terms of nodal efficiency and intra-modular communication. ...
Article
Full-text available
Connectivity‐based parcellation (CBP) methods are used to define homogenous and biologically meaningful parcels or nodes—the foundations of brain network fingerprinting—by grouping voxels with similar patterns of brain connectivity. However, we still lack a gold standard method and the use of CBPs to study the aging brain remains scarce. Our study proposes a novel CBP method from diffusion MRI data and shows its potential to produce a more accurate characterization of the longitudinal alterations in brain network topology occurring in aging. For this, we constructed whole‐brain connectivity maps from diffusion MRI data of two datasets: an aging cohort evaluated at two timepoints (mean interval time: 52.8 ± 7.24 months) and a normative adult cohort—MGH‐HCP. State‐of‐the‐art clustering techniques were used to identify the best performing technique. Furthermore, we developed a new metric (connectivity homogeneity fingerprint [CHF]) to evaluate the success of the final CBP in improving regional/global structural connectivity homogeneity. Our results show that our method successfully generates highly homogeneous parcels, as described by the significantly larger CHF score of the resulting parcellation, when compared to the original. Additionally, we demonstrated that the developed parcellation provides a robust anatomical framework to assess longitudinal changes in the aging brain. Our results reveal that aging is characterized by a reorganization of the brain's structural network involving the decrease of intra‐hemispheric, increase of inter‐hemispheric connectivity, and topological rearrangement. Overall, this study proposes a new methodology to perform accurate and robust evaluations of CBP of the human brain.
... La régulation émotionnelle nécessiterait la mobilisation d'un contrôle cognitif et dépendrait ainsi des ressources disponibles (Knight et al., 2007). De nombreuses études en neuro-imagerie ont validé le biais de positivité chez la personne âgée et l'explique par une réduction de l'activité de l'amygdale couplée à une augmentation de l'activité du CPF lors du traitement de stimuli négatifs (Mather, 2012;Nashiro et al., 2012). Des études ont montré que, comparé à celui de jeunes adultes, le traitement de stimuli négatifs chez les adultes âgés était associé à une augmentation de l'activité du CF (Tessitore et al., 2005). ...
Thesis
Ce travail de thèse visait d’une part à décrire les paramètres oculomoteurs, d’autre part à analyser les patterns d’exploration visuelle associés aux conduites suicidaires chez les personnes âgées dépressives. À travers une série de trois articles, nous avons examiné les liens entre processus cognitifs et saccades oculaires (Articles 1 et 2). Par ailleurs, nous avons également étudié le traitement de l'information émotionnelle lors de la présentation de visages expressifs (Article 3). La comparaison directe des performances oculomotrices de patients âgés dépressifs avec conduites suicidaires et de patients dépressifs non suicidaires a permis de caractériser des performances oculomotrices spécifiques aux conduites suicidaires. Enfin, nous avons pu mettre en évidence la spécificité de l’analyse visuelle des informations émotionnelles des visages chez des patients âgés dépressifs avec conduites suicidaires. Dans l‘ensemble, nos travaux ont montré une influence du déclin cognitif lié aux conduites suicidaires sur les performances oculomotrices. Les performances de saccades oculaires étaient différentes chez les patients avec conduites suicidaires qui présentaient un pourcentage significativement plus faible d’antisaccades corrigées ainsi que des temps de correction plus élevés en antisaccades. Ces résultats pourraient suggérer un déficit exécutif plus important, notamment au niveau de la flexibilité, chez les personnes suicidaires. De plus, le traitement des stimuli émotionnels a révélé des stratégies particulières chez les personnes âgées dépressives avec des conduites suicidaires. Nous avons observé des temps de fixation plus longs sur les caractéristiques émotionnelles (c'est-à-dire les yeux et la bouche) en réponse à la peur, au dégoût et aux visages neutres. A travers des tâches de saccades ou d‘exploration visuelle, les mouvements oculaires pourraient refléter les processus cognitifs sous-jacents aux conduites suicidaires chez les personnes âgées dépressives et permettre d’identifier des facteurs cognitifs de risque du suicide
... The SST theory thus argues for a more top-down, controlled shift in attentional resources toward goal-relevant (i.e., positive) stimuli in older individuals. The cognitive control hypothesis (CCH) (Nashiro et al., 2012) argues that older adults' preference for emotional wellbeing results from their increased devotion of cognitive resources to emotion regulation. Empirically, supporting CCH, older adults had more medial prefrontal cortex (mPFC) activity for positive pictures than negative ones, when they were deeply engaged in the task (Ritchey et al., 2011). ...
Article
Older adults often show a positivity bias effect during picture processing, focusing more on positive than negative information. It is unclear whether this positivity bias effect generalizes to language and whether arousal matters. The present study investigated how age affects emotional word comprehension with varied valence (positive, negative) and arousal (high, low). We recorded older and younger participants’ brainwaves (EEG) while they read positive/negative and high/low-arousing words and pseudowords, and made word/non-word judgments. Older adults showed increased N400s and left frontal alpha decreases (300–450 ms) for low-arousing positive as compared to low-arousing negative words, suggesting an arousal-dependent positivity bias during lexical retrieval. Both age groups showed similar LPPs to negative words. Older adults further showed a larger mid-frontal theta increase (500–700 ms) than younger adults for low-arousing negative words, possibly indicating down-regulation of negative meanings of low-arousing words. Altogether, our data supported the strength and vulnerability integration model of aging.
... Older adults show increased use of distancing (i.e., appraising an emotional situation as an objective, rational observer) and reappraisal (i.e., reinterpreting a stimulus to change one's emotional response to it) [96]. Enhancement of emotion regulation strategies with age may be a driving factor of the positivity effect [97]. Older adults with subjective memory complaints have reduced emotion regulation capabilities, suggesting that declines in emotion regulation could be an early sign of age-related degeneration [98]. ...
Article
Full-text available
Purpose of Review This review aims to summarize current research on the psychological and neural substrates of emotion and memory in aging. Recent Findings Emotional memory remains largely intact with age; however, there are mixed findings regarding what type of information is preserved. Shifts in functional connectivity in the medial temporal lobe (MTL) and frontal cortex may underlie emotional memory alterations in aging and are particularly vulnerable to age-related disorders. However, we may be able to harness the interaction between emotion and memory to alleviate memory dysfunction in late life. Summary The relationship between emotion and memory in aging is complex, as emotional biases exist but may differ depending on factors such as underlying pathology or stress hormones. With the advent of advanced imaging methodology and sensitive cognitive tasks, we are better suited to address these research questions. Understanding how emotion may be harnessed to modulate memory may provide a mechanism to rescue memory deficits in aging and disease.
... In this meta-analysis, we included adult patients aged between 18 and 60 years in order to exclude the potential effect of adolescent and aged brains on the neural correlates of reappraisal (Ahmed, Bittencourt-Hewitt, & Sebastian, 2015;Lantrip & Huang, 2017;Nashiro, Sakaki, & Mather, 2012). However, emotion regulation is a dynamic process and may change across the lifespan (Consedine & Mauss, 2014;Livingstone & Isaacowitz, 2021). ...
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