Effects of aging on functional connectivity of the amygdala during negative evaluation: a network analysis of fMRI data

Abstract

Previous evidence has suggested both preserved emotional function in aging and age-related differences in emotional processing, but the neural networks underlying such processing alterations in the context of preserved affective function are not clear. Using event-related fMRI, we scanned young and older adults while they made valence ratings for emotional pictures. Behavioral results showed a similar pattern of emotional evaluation, but older adults experienced negatively valenced pictures as being less negative. Consistent with behavioral findings, we identified common activity in the right amygdala, but age-related differences in the functional connectivity of this region with the rest of the brain. Compared to young adults, older adults had greater functional connectivity between the right amygdala and ventral anterior cingulate cortex, possibly reflecting increased emotional regulation. Conversely, older adults showed decreased functional connectivity with posterior brain regions, likely reflecting decreased perceptual processing. Thus, age-related differences in evaluating negatively valenced stimuli might reflect decreased perceptual processing of these stimuli, as well as the engagement of control processes that inhibit the response to negative emotion.

Fig. 1. Negative-to-neutral shift

Participant ratings for negative pictures. Bars represent the mean proportion of the overlap between participants’ ratings of negative and neutral that corresponds to the standardized ratings for negative pictures. Young adults rated a higher proportion of negative pictures (according to the standard) as negative, whereas older adults rated a higher proportion of negative pictures (according to the standard) as neutral. Error bars indicate the standard deviation.

Fig. 2. Common amygdala activation

Common emotional evaluation in the right amygdala from the conjunction analysis based on a region of interest approach, where both young and older groups showed common activity for negative versus neutral stimuli (P = .0025). The y-axis represents the difference in activity between negative and neutral conditions and units are in effect size, the difference in the parameter estimates of the activation.

Fig. 3. Age-related differences in functional connectivity

Age-related differences in the emotional network for negative pictures, showing a Posterior–Anterior Shift in Aging (approaches P = .000125). Older adults had enhanced functional connectivity between the right amygdala and anterior brain regions (ACC), and reduced functional connectivity between the right amygdala and posterior brain regions. The y-axis represents the difference in correlations between negative and neutral conditions. ACC: anterior cingulate cortex.

Fig. 4. Amygdala and ventral ACC connectivity

(A) Functional connectivity between the right amygdala and ventral ACC in older adults for the overall negative condition compared to a subset of older adults for the negative-to-neutral shift, negative pictures subjectively rated as neutral (negative-neutral). ACC: anterior cingulate cortex. (B) Reduction of amygdala activity in a subset of older adults for the negative-to-neutral shift (negative-neutral) compared to the overall negative condition.