Cognitive and neural contributors to emotion regulation in aging

Abstract

Older adults, compared to younger adults, focus on emotional well-being. While the lifespan trajectory of emotional processing and its regulation has been characterized behaviorally, few studies have investigated the underlying neural mechanisms. Here, older adults (range: 59-73 years) and younger adults (range: 19-33 years) participated in a cognitive reappraisal task during functional magnetic resonance imaging (fMRI) scanning. On each trial, participants viewed positive, negative or neutral pictures and either naturally experienced the image ('Experience' condition) or attempted to detach themselves from the image ('Reappraise' condition). Across both age groups, cognitive reappraisal activated prefrontal regions similar to those reported in prior studies of emotion regulation, while emotional experience activated the bilateral amygdala. Psychophysiological interaction analyses revealed that the left inferior frontal gyrus (IFG) and amygdala demonstrated greater inverse connectivity during the 'Reappraise' condition relative to the 'Experience' condition. The only regions exhibiting significant age differences were the left IFG and the left superior temporal gyrus, for which greater regulation-related activation was observed in younger adults. Controlling for age, increased performance on measures of cognition predicted greater regulation-related decreases in amygdala activation. Thus, while older and younger adults use similar brain structures for emotion regulation and experience, the functional efficacy of those structures depends on underlying cognitive ability.

Figures

Fig. 1

Cognitive reappraisal task. Participants were trained in the use of a reappraisal strategy for emotion regulation. (A) On ‘Experience’ trials, participants viewed an image then received an instruction to experience naturally the emotions evoked by that image. The image then disappeared, but participants continued to experience their emotions throughout a 6-s delay period. At the end of the trial, the participants rated the perceived affective valence of that image using an 8-item Likert scale. (B) ‘Reappraise’ trials had similar timing, save that the cue instructed participants to decrease their emotional response to the image by reappraising the image (e.g. distancing oneself from the scene). Shown are examples of the negative (A) and positive (B) images used in the study.

Fig. 2

Valence ratings across task conditions. Both older and younger adults reported significant emotion regulation: the ‘Experience’ (Exp) trials led to more extreme valence ratings than the ‘Reappraise’ (Reap) trials, for both groups.

Fig. 3

Neural correlates of cognitive reappraisal and emotional experience. (A) The contrast of ‘Reappraise’ >‘Experience’, collapsed over conditions and age groups, revealed that activation in dlPFC, dmPFC and the IPL increased when participants engaged in reappraisal. (B) Conversely, the contrast of ‘Experience’ >‘Reappraise’ revealed that activation in the amygdala was decreased by reappraisal. Similar effects were observed for both negative-valenced (left images) and positive-valenced (right images) stimuli.

Fig. 4

Modulation of prefrontal and amygdalar activation by emotion regulation. (A) Examination of a functional region of interest in the LIFG revealed a pattern of activation that followed subjects’ self-reports of emotion regulation. Shown here are voxels activated in the contrast between ‘Reappraise-Negative’ and ‘Experience-Negative’ conditions. (B) For both positive and negative stimuli, and for both younger and older adults, LIFG activation increased to ‘Reappraise’ trials compared to ‘Experience’ trials. (C) Conversely, a functional region of interest comprising the bilateral amygdala (Amy) revealed a systematic decrease in activation under emotion regulation. Shown are voxels activated in the contrast between ‘Experience-Negative’ and ‘Reappraise-Negative’ conditions. (D) For both positive and negative stimuli, and for both younger and older adults, amygdala activation increased to ‘Experience’ trials compared to ‘Reappraise’ trials.

Fig. 5

A PPI between amygdala and lateral prefrontal cortex. We conducted a PPI analysis using each of the left and right amygdala as seed regions, and the regulation condition (‘Reappraise’ or ‘Experience’) as a modulatory variable. Significant PPI effects were observed in the left prefrontal cortex, with a region of overlap in the LIFG. These results indicate that emotion regulation modulates the functional connectivity between the amygdala and the LIFG.

Fig. 6

Age differences in the modulation of lateral prefrontal cortex by emotion regulation. A whole-brain analysis identified brain regions for which the contrast between ‘Reappraise’ and ‘Experience’ conditions was significantly different between younger and older adults. (A) We found one region for which there was greater activation for younger compared to older adults, for regulation of negative emotions: the LIFG. (B) Within this region, young adults exhibited significantly greater activation during ‘Reappraise’ compared to ‘Experience’ trials, whereas older adults showed no differences between those conditions.

Fig. 7

Partial correlations between cognitive ability and regulation-related activation in the amygdala. For functional regions of interest in prefrontal cortex and the amygdala, we examined whether individual differences in cognitive abilities predicted regulation-induced changes in activation. We assessed cognition through a battery that tested aspects of memory and processing speed. Partial correlation analyses evaluated the relationship between composite cognitive scores and changes in activation between the ‘Reappraise’ and ‘Experience’ conditions, after controlling for any effects of age itself. Shown are leverage scatterplots of the relationships between age-controlled cognitive battery z scores and age-controlled activation in the left (A) and right (B) amygdala. For both regions, increased cognitive ability predicted greater decreases in activation under conditions of emotion regulation.