Edited by: Natalie Ebner, University of Florida, USA
Reviewed by: Hakan Fischer, Stockholm University, Sweden; Heather L. Urry, Tufts University, USA; Anne Krendl, Indiana University Bloomington, USA
*Correspondence: Sanda Dolcos, Department of Psychology, University of Illinois at Urbana-Champaign, 603 E. Daniel Street, Champaign, IL 61820, USA e-mail:
This article was submitted to Emotion Science, a section of the journal Frontiers in Psychology.
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Despite ample support for enhanced affective well-being and emotional stability in healthy aging, the role of potentially important dimensions, such as the emotional arousal, has not been systematically investigated in neuroimaging studies. In addition, the few behavioral studies that examined effects of arousal have produced inconsistent findings. The present study manipulated the arousal of pictorial stimuli to test the hypothesis that preserved emotional functioning in aging is modulated by the level of arousal, and to identify the associated neural correlates. Young and older healthy participants were presented with negative and neutral pictures, which they rated for emotional content, while fMRI data were recorded. There were three main novel findings regarding the neural mechanisms underlying the processing of negative pictures with different levels of arousal in young and older adults. First, the common engagement of the right amygdala in young and older adults was driven by high arousing negative stimuli. Second, complementing an age-related reduction in the subjective ratings for low arousing negative pictures, there were opposing patterns of activity in the rostral/ventral anterior cingulate cortex (ACC) and the amygdala, which showed increased vs. decreased responses, respectively, to low arousing negative pictures. Third, increased spontaneous activity in the ventral ACC/ventromedial prefrontal cortex (vmPFC) in older adults was linked to reduced ratings for low arousing negative pictures. Overall, these findings advance our understanding of the neural correlates underlying processing of negative emotions with different levels of arousal in the context of enhanced emotional functioning in healthy aging. Notably, the results support the idea that older adults have emotion regulation networks chronically activated, in the absence of explicit induction of the goal to regulate emotions, and that this effect is specific to low arousing negative emotions.
Aging is associated with well-known co-morbidities and losses, but also with relatively high levels of emotional well-being. The idea of relatively well-preserved emotional processing in aging is supported by evidence showing that older adults tend to (a) pay attention to and remember more positive information (Charles et al.,
Prominent models of emotion identify valence and arousal as fundamental components of emotion (see Bradley and Lang,
Previous evidence has shown that processing of low and high arousing emotional stimuli relies on distinct processes. On the one hand, low arousing negative stimuli activate more goal-driven processes, which tend to engage controlled, resource-demanding processes (Kensinger and Corkin,
A more probable explanation for the inconsistent findings regarding age-related differences in amygdala activation to negative stimuli may be that the pictures used in those studies differed in emotional arousal. This explanation is in line with previous evidence in older adults showing (a) preserved amygdala responses to positive (Mather et al.,
Decreased amygdala activity, combined with increased activity in emotion control regions, such as the medial PFC and the adjacent anterior cingulate cortex (ACC), might also be the result of a greater focus on emotion regulation goals. According to the Socioemotional Selectivity Theory (SST; Scheibe and Carstensen,
This interpretation is consistent with studies showing interactions between similar medial PFC/ACC regions and the amygdala, when older adults voluntarily decreased emotional responses to negative stimuli (Urry et al.,
The present event-related fMRI study used a broader range of negative emotional stimuli (low, medium, and high arousing) to test the hypothesis that emotional functioning in aging is modulated by the level of arousal, and to identify the associated neural correlates. The focus was on the ACC/vmPFC and the amygdala. Participants were presented with negative and neutral pictures, which they rated for emotional content, while fMRI data were recorded. Based on the above review, we made the following four predictions. First, from the evidence showing a negative-to-neutral shift in older adults' ratings, we predicted lower ratings to the low arousing negative pictures in older adults. Second, we predicted that common engagement of the amygdala in young and older adults would be specific to high arousing pictures, reflecting preserved responses to high arousing stimuli in older adults. Third, we predicted that opposing patterns of response in the ACC/vmPFC (increased) vs. amygdala (decreased) would be specific to low arousing stimuli. Finally, consistent with a role of the vACC/vmPFC in spontaneous emotional regulation, we explored the possibility that increased activity in this region would be linked to reduced ratings for low arousing negative stimuli in older adults.
The subject sample comprised 18 young adults between the ages of 18 and 32 years (10 females, mean age = 23.61,
18 | 16 | ||
Male/Female | 8/10 | 5/11 | |
Age range | 18–32 | 59–84 | |
Mean age ( |
23.61 (4.19) | 68.56 (6.98) | <0.001 |
Years of education ( |
14.11 (2.22) | 14.19 (2.97) | 0.99 |
Stimuli presented during the scanning session consisted of 180 pictures (90 negative and 90 neutral) selected from the IAPS (Lang et al.,
The focus on negative emotional pictures in the present study was justified by the following reasons. First, previous evidence shows that the influence of arousal on age differences is more pronounced for negative than for positive stimuli (Kensinger,
The pool of 180 pictures was divided into sets of 30 pictures (15 negative and 15 neutral pictures in each set), which were randomly assigned to six study blocks. The block orders were randomly assigned to the participants. To avoid mood induction, pictures were pseudo-randomized so that no more than three pictures of the same valence were consecutively presented. Functional MR images were recorded while participants viewed and rated negative and neutral images. Each picture was presented on the screen for 4 s, and then was removed to minimize confounding effects of eye movements associated with prolonged scanning of images. Participants were asked to watch the pictures and rate their subjective emotional experience triggered by the pictures on an 8-point scale (1 = neutral, 8 = extremely negative). The rating scale was presented at the bottom of each picture. The screen containing the picture and rating scale was followed by a fixation cross, presented on the screen for 12 s. Participants were instructed to rate the pictures only after they were aware of the content of the picture and of their emotional response to the picture. Participants were encouraged to try and rate the pictures while they were on the screen. However, participants were also told to respond during the fixation screen if they needed more time to rate the picture. Participants first completed a run in which they were instructed to experience any feelings or thoughts the pictures might trigger. The first run was intended to collect data on participants' spontaneous processing and evaluation of negative information with varying degrees of arousal. The following runs were intended to collect data on participants' responses following the induction of the goal to regulate emotion (Dolcos et al.,
fMRI data were recorded using a 1.5 Tesla Siemens Sonata scanner. The anatomical images were 3D MPRAGE anatomical series (repetition time,
Standard pre-processing steps included quality assurance, TR alignment, motion correction, co-registration, normalization and smoothing (8 mm full-width half maximum isotropic kernel). Motion parameters calculated during the realignment were included as parameters of no interest to control for movement artifacts. For individual analyses, each event was modeled by the canonical hemodynamic response function (hrf) and its temporal derivative. The hemodynamic response can potentially show age-related differences (for review, see Dennis and Cabeza,
The main goal of the study was to investigate age-related differences in the neural correlates of evaluating emotional information with different levels of arousal. The focus was on the role of regions involved in basic emotion processing (amygdala) and emotion control (ACC/vmPFC). To accomplish this goal, analyses were performed to identify the common set of brain regions engaged by both young and older adults, through conjunction analyses. To examine our a priori hypothesis regarding the amygdala, we used anatomical ROI masks derived from the Wake Forest University Pick Atlas toolbox (Dolcos et al.,
Further analyses were performed to identify dissociable sets of brain regions showing greater sensitivity to negative than to neutral pictures across groups, using ANOVAs and two-sample
First, a Valence (Negative and Neutral) × Age Group (Young and Older) repeated-measures ANOVA with Valence as a within-subject factor and Age Group as a between-subjects factor revealed a main effect of Valence [
NegHi | 6.55 (1.08) | 5.68 (1.82) | 1.68 | 0.106 |
NegMed | 5.58 (1.38) | 5.18 (1.59) | 0.80 | 0.425 |
NegLo | 4.62 (1.29) | 3.89 (1.19) | 1.72 | 0.096 |
1.56 | 0.128 | |||
0.55 | 0.584 |
Conjunction analyses of brain activity associated with the evaluation of negative and neutral pictures identified an area in the right amygdala that was commonly engaged by both age groups (see Table
Amygdala | R | 6 | 28 | −1 | −20 | |
Amygdala | L | 6 | −20 | −5 | −17 | |
Amygdala | R | 22 | 16 | −5 | −17 | |
28 | −1 | −20 |
Cuneus | 18 | R | 26 | 12 | −85 | 19 | 4.26 | |
8 | −92 | 19 | 3.71 | |||||
Precuneus | 19 | R | 12 | 28 | −60 | 36 | 3.94 | |
Middle temporal gyrus | 19 | R | 21 | 48 | −61 | 14 | 3.85 | |
Cingulate gyrus | 32 | L | 17 | −4 | 17 | 32 | 3.69 | |
Postcentral gyrus | 2 | R | 10 | 51 | −21 | 42 | 3.66 | |
Middle temporal gyrus | 19 | L | 18 | −44 | −61 | 14 | 3.60 | |
Middle temporal gyrus | 37 | −51 | −62 | 3 | 2.83 | |||
Middle occipital gyrus | 18 | L | 21 | −32 | −89 | 4 | 3.47 | |
−24 | −89 | 15 | 3.38 | |||||
Amygdala | 34 | L | 11 | −20 | −1 | −10 | 2.49 |
|
−32 | −5 | −17 | 2.10 |
|||||
Amygdala | 28 | R | 18 | 16 | −4 | −10 | 2.44 |
|
34 | 28 | 3 | −14 | 1.96 |
||||
Inferior frontal gyrus | 47 | R | 34 | 44 | 11 | −4 | 4.81 | |
Superior temporal gyrus | 41 | R | 13 | 40 | −35 | 9 | 4.02 | |
48 | −31 | 5 | 3.17 | |||||
40 | −38 | 16 | 2.82 | |||||
Middle temporal gyrus | 39 | R | 23 | 48 | −61 | 21 | 3.85 | |
44 | −54 | 14 | 3.31 | |||||
48 | −62 | 10 | 2.99 | |||||
Superior frontal gyrus | 9 | R | 26 | 40 | 40 | 31 | 3.79 | |
16 | 52 | 38 | 3.78 | |||||
4 | 56 | 38 | 3.67 | |||||
Superior frontal gyrus | 9 | L | 22 | −28 | 52 | 34 | 3.77 | |
−12 | 52 | 38 | 3.62 | |||||
Middle occipital gyrus | 19 | L | 14 | −28 | −77 | 11 | 3.75 | |
−32 | −85 | 8 | 3.43 | |||||
−24 | −89 | 15 | 3.09 | |||||
Inferior frontal gyrus | 47 | L | 20 | −48 | 42 | −9 | 3.75 | |
−51 | 30 | −5 | 2.94 | |||||
−55 | 35 | 2 | 2.86 | |||||
Middle frontal gyrus | 8 | R | 32 | 36 | 22 | 47 | 3.68 | |
48 | 21 | 39 | 3.67 | |||||
32 | 6 | 58 | 3.25 | |||||
Superior temporal gyrus | 38 | L | 40 | −44 | 11 | −14 | 3.64 | |
−40 | 23 | −11 | 3.47 | |||||
−51 | 7 | −7 | 3.32 | |||||
Anterior cingulate gyrus | 32 | L | 39 | −16 | 36 | 13 | ||
−12 | 43 | −2 | 2.42 | |||||
32 | R | 8 | 8 | 40 | 16 | 1.88 |
Confirming our third prediction, targeted two-sample
ACC | NegHi | 1.35 (1.42) | −4.93 (2.27) |
NegMed | −4.91 (2.08) | −3.08 (1.98) | |
NegLo | −4.29 (1.48) | 2.39 (1.35) | |
NeuAll | −1.78 (1.83) | −4.68 (1.60) | |
AMY | NegHi | 22.93 (7.18) | 12.88 (4.92) |
NegMed | 15.18 (5.07) | 2.34 (4.34) | |
NegLo | 15.83 (4.44) | −0.93 (3.96) | |
NeuAll | 6.74 (2.29) | 4.12 (3.20) |
Co-variations of activity in the vACC/vmPFC with the behavioral ratings further elucidated the role played by this region in the evaluation of low arousing stimuli in older adults (see Figure
(NegHi vs. NeuAll) × NegHi | −0.668 | Inferior frontal gyrus | 47 | L | 10 | −20 | 31 | −5 | 3.59 |
(NegLo vs. NeuAll) × NegLo | −0.726 | Parahippocampal gyrus | 35 | L | 14 | −20 | −35 | −5 | 4.22 |
(NegHi vs. NeuAll) × NegHi | +0.803 | Precuneus | 7 | L | 56 | −4 | −53 | 43 | 5.04 |
+0.770 | 0 | −45 | 28 | 4.52 | |||||
+0.705 | 7 | R | 12 | −52 | 43 | 3.72 | |||
+0.778 | Precentral gyrus | 9 | L | 12 | −36 | 21 | 39 | 4.64 | |
+0.769 | Superior parietal lobule | 7 | R | 16 | 28 | −68 | 44 | 4.50 | |
+0.746 | Precuneus | 7 | L | 10 | −12 | −59 | 55 | 4.19 | |
+0.722 | −12 | −68 | 51 | 3.90 | |||||
+0.707 | Medial frontal gyrus | 8 | 12 | 0 | 45 | 38 | 3.74 | ||
+0.707 | 0 | 56 | 30 | 3.74 | |||||
+0.669 | Medial frontal gyrus | 9 | L | −4 | 40 | 31 | 3.37 | ||
+0.690 | Superior frontal gyrus | 9 | L | 14 | −8 | 60 | 26 | 3.57 | |
+0.679 | R | 8 | 63 | 15 | 3.45 | ||||
(NegMed vs. NeuAll) × NegMed | −0.819 | Inferior parietal lobule | 40 | L | 11 | −40 | −29 | 42 | 5.34 |
−0.686 | −28 | −37 | 42 | 3.52 | |||||
−0.797 | Precentral gyrus | 6 | R | 10 | 32 | −9 | 56 | 4.94 | |
−0.783 | Precentral gyrus | 6 | L | 26 | −24 | −10 | 52 | 4.70 | |
−0.699 | −16 | −1 | 55 | 3.65 | |||||
−0.699 | −24 | −1 | 48 | 3.65 | |||||
−0.777 | Precentral gyrus | 6 | L | 13 | −55 | −2 | 41 | 4.62 | |
−0.774 | Precuneus | 7 | R | 26 | 8 | −59 | 62 | 4.58 | |
−0.668 | 4 | −56 | 51 | 3.35 | |||||
−0.751 | Precuneus | 7 | L | 11 | −28 | −71 | 55 | 4.25 | |
−0.749 | Caudate nucleus | R | 20 | 4 | 8 | 0 | 4.23 | ||
−0.711 | L | −4 | 4 | −4 | 3.79 | ||||
−0.739 | Lentiform nucleus | R | 19 | 20 | −4 | 8 | 4.11 | ||
−0.712 | Inferior parietal lobule | 40 | L | 21 | −44 | −36 | 57 | 3.79 | |
−0.700 | −40 | −47 | 61 | 2.67 | |||||
−0.710 | Superior temporal gyrus | 22 | R | 10 | 60 | −7 | 8 | 3.77 | |
−0.708 | 51 | 4 | 7 | 3.75 | |||||
−0.675 | 48 | 5 | 15 | 3.43 | |||||
(NegLo vs. NeuAll) × NegLo | +0.750 | Insula | 13 | R | 12 | 28 | −26 | 23 | 4.24 |
+0.743 | 36 | −45 | 28 | 4.22 | |||||
+0.767 | 32 | −34 | 24 | 4.04 | |||||
+0.711 | Supramarginal gyrus | 40 | L | 11 | −44 | −45 | 32 | 4.16 | |
+0.653 | Superior frontal gyrus | 8 | R | 10 | 4 | 37 | 46 | 3.53 | |
(NegLo vs. NeuAll) × NegLo | −0.577 | Anterior cingulate | 32 | R | 7 | 0 | 38 | −9 | 4.11 |
Despite substantial evidence supporting the idea of enhanced affective well-being and emotional stability in healthy aging, relatively little is known about the role of emotional arousal in this effect and the underlying brain mechanisms. The current study addressees this gap in the emotional aging literature by investigating the effect of emotional arousal on behavioral and neural responses in young and older adults. There were three main novel findings regarding the neural correlates. First, we showed that the common engagement of the right amygdala in young and older adults was driven by high arousing stimuli. Second, we showed that the opposing spontaneous pattern of increased activity in the rostral/ventral ACC and decreased activity in the right amygdala is specific to low arousing stimuli. Third, we linked the increased spontaneous activity in the vACC/vmPFC to older adults' reduced ratings for low arousing stimuli. These findings are discussed below.
The present study revealed that right amygdala activation in older adults had overlapping areas with that from younger adults, thus showing that both groups involve the same amygdala regions to process negative stimuli. Moreover, the present study advances previous findings (St. Jacques et al.,
The present results are also in line with more recent theories of emotional aging (cognitive control model: Mather and Carstensen,
The present study also advances previous findings by showing that the age-related differences in the engagement of amygdala and rostral/ventral ACC are specific to low arousing negative stimuli. Older adults' reduced amygdala activation to low arousing negative pictures can be the consequence of many factors, including an age-related atrophy in neural systems important for processing negative stimuli, age-related decreases in psychophysiological responses to arousing stimuli (Tsai et al.,
Taken together, our findings show enhanced activity in an emotional control region, the rostral/ventral ACC, coupled with decreased bilateral amygdala activity to low arousing negative stimuli, in a task in which participants were not explicitly instructed to down-regulate their emotional responses. This may reflect older adults' spontaneous engagement of emotion control regions to down-regulate low arousing negative emotions. Moreover, the negative association between vACC/vmPFC and behavioral ratings for low arousing stimuli, discussed below, reflects their success in regulating low arousing negative emotions. These results support the idea that older adults may have emotion regulation chronically activated (Mather and Carstensen,
Ventromedial PFC and the ACC play an important role in processing emotional information, and are particularly involved in the automatic regulation of emotional responses (for reviews see Bush et al.,
Although our study contributes important novel information, it also has some limitations. One limitation concerns the size of our subject sample in the older group, which although allowed identification of robust findings, was slightly smaller than the optimal fMRI sample size of 18 suggested for investigations of brain-behavior relations (Lieberman et al.,
In the present study, we examined the effect of arousal as a potential factor influencing the enhanced affective well-being and emotional stability commonly associated with healthy aging. There were three novel findings regarding the neural correlates of emotion processing: (a) right amygdala was commonly engaged by young and older adults only during the evaluation of high arousing stimuli, (b) amygdala and rostral/ventral ACC showed an opposing pattern of activity for low arousing stimuli in older compared to young adults, and (c) the engagement of the ventral ACC/vmPFC in older adults reflected successful regulation of low arousing negative stimuli. These findings highlight the important effect of arousal on age-related emotional processing, suggesting that aging is associated with preserved emotional processing of high arousing negative information, and with altered processing of low arousing negative information. By showing that older adults engage more automatic processes when evaluating high arousing negative information, and more controlled, resource-demanding processes in response to low arousing negative information, the present study advances our understanding of the neural correlates underlying the enhanced emotional well-being in healthy aging. Moreover, by linking the spontaneous engagement of the emotion control regions in older adults to reduced subjective experiencing of low arousing negative information, the present study provides further evidence supporting the idea that emotion regulation is chronically activated in healthy aging, and clarifies that this effect is specific to low arousing negative information. This new evidence highlights the need of adopting a comprehensive approach that takes into consideration both the valence and arousal in examining emotional aging.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
This research was supported by funds from the Brain & Behavior Research Foundation (formerly NARSAD), Healthy Minds Canada (formerly CPRF), and the University of Alberta. The authors were supported by NIH R01 grant AG008235 from the National Institutes of Health (National Institute on Aging) (Roger A. Dixon and Sanda Dolcos), the Canada Research Chairs program (Roger A. Dixon), the University of Alberta (Sanda Dolcos and Roger A. Dixon), and the University of Illinois (Sanda Dolcos). The authors wish to thank Keen Sung, Trisha Chakrabarty, and Kristina Suen for assistance with data collection and analysis, and to Florin Dolcos for feedback on an earlier version of the manuscript.