Inhibition of emotions in healthy aging: age-related differences in brain network connectivity

Abstract

Introduction: Successful inhibition of distracting emotions is important for preserving well-being and daily functioning. There is conflicting evidence regarding the impact of healthy aging on emotional inhibition, and possible age-related alterations in the neuronal underpinnings of emotional interference processing are unexplored.

Methods: Thirty younger (mean age 26 years; 15 women) and 30 older (mean age 71 years; 13 women) healthy adults performed a face-word emotional Stroop task while undergoing functional magnetic resonance imaging of the brain. A resting-state scan was acquired for calculating the amplitude of low-frequency fluctuations as an estimate of vascular reactivity. Comparisons of brain activation during the task were assessed in a whole-brain, voxel-wise analysis, contrasting congruent, and incongruent conditions. The canonical regions of the frontoparietal, salience, dorsal attention, and default mode networks were used as seed regions for assessing functional connectivity within and between large-scale brain networks. Task performance was evaluated using response accuracy and response time.

Results: The older adults had longer response times and lower task accuracy than the younger adults, but the emotional interference effect was not significantly different between the groups. Whole-brain analysis revealed no significant age-related differences in brain activation patterns. Rescaling the data for estimated variability in vascular reactivity did not affect the results. In older adults, there was relatively stronger functional connectivity with the default mode network, the sensorimotor network, and the dorsal attention network for the frontoparietal and salience network seeds during the task. Conversely, younger adults had relatively stronger connections within and between the frontoparietal and salience networks.

Conclusion: In this first fMRI study of emotional Stroop interference in older and younger adults, we found that the emotional interference effect was unchanged in healthy aging and replicated the finding from non-emotional task studies that older adults have greater between-network and less within-network connectivity compared to younger adults.

Keywords: aging; connectome; emotions; fMRI; inhibition.

FIGURE 1

Illustration of the face/word emotional Stroop task (eStroop)

FIGURE 2

Performance in the eStroop task. The figure displays mean response times (RTs) for all correct trials (a) and mean accuracy (ACC) (b) in the two age groups separately for congruent, incongruent, and all trials, as well as the comparisons between the means within and between groups (*p < 0.05, **p < 0.001, n.s. = non‐significant). The error bars represent the 95%‐confidence intervals for the means. The x‐axes are cropped at 500 ms in (a) and 90% in (b) to improve visibility

FIGURE 3

Results of the voxel‐wise one‐sample t test for the incongruent > congruent contrast across all 60 participants. Nonparametric correction for multiple comparisons using randomization with 10,000 permutations, FWE‐corrected p < 0.05, t‐threshold 4.41

FIGURE 4

Connectograms displaying connections with significantly higher (warm colors) or lower (cool colors) connectivity for older compared with younger adults during incongruent trials with (a) frontoparietal network seeds, (b) dorsal attention network seeds, (c) salience network seeds, and (d) default mode network seeds. p‐value FDR‐corrected < 0.05

FIGURE 5

Correlations between the connectivity measures that were significantly different between age groups, within and between the frontoparietal, dorsal attention and salience networks and between these networks and the default mode and sensorimotor networks. Correlations within the younger group and within the older group are shown above and below the diagonal, respectively. Nominally significant correlations are color‐coded, and FDR‐corrected significant correlations are marked with an X