Abstract
Amygdala activity was previously found to correlate with neuroticism as an effect of valence, but so far few studies have focused on motivational context. The network subserving altered amygdala activity has not yet been investigated although some studies showed strong effective connections with prefrontal cortex (PFC). The goal of this study was to test the modulatory role of neuroticism on the functional connectivity (FC) between amygdala and other brain regions, especially PFC, during emotion processing from motivational direction. We applied an emotional picture viewing paradigm with different motivational directions (approaching and avoiding) in a large participant sample. The results showed that neuroticism predicted the amount of amygdala FC to dorsomedial PFC (dmPFC) and middle cingulate cortex (MCC). Increased FC during negative vs. positive pictures was found primarily in low neuroticism subjects, especially during the avoid condition. This valence and motivation dependent connectivity increase were disrupted for high neurotic participants. No effect of neuroticism was found for the approach condition. We showed that neuroticism, especially in the context of passive affect regulation, may have impaired connectivity between amygdala and putative regulatory cortical networks.
Highlights
Neuroticism is one of the Big Five dimensions of personality traits (Digman, 1990) and individuals who score high on neuroticism showed a strong tendency to experience negative affection, such as anxiety, worry, fear, anger, frustration, envy, jealousy, guilt, depressive mood and loneliness, especially when threatened, frustrated, or facing loss (Thompson, 2008; for review, see Ormel et al, 2013a)
Motivation-Independent functional connectivity (FC) We found a significant stronger FC between right amygdala and right middle cingulate cortex (MCC; t42 = 4.13, p = 0.027 family-wise error (FWE) correction; MNI: 18, −16, 41; cluster size = 153) when processing the positive pictures compared to negative pictures, which is more evident in high neurotic individual than low neurotic individuals
For the negative < positive contrast, we found a stronger FC between the right amygdala and dorsomedial PFC (dmPFC) in high compared to low neurotic individuals (t42 = 5.20, p < 0.001 FWE correction; MNI: −6, 50, 35; cluster size = 389)
Summary
Neuroticism is one of the Big Five dimensions of personality traits (Digman, 1990) and individuals who score high on neuroticism showed a strong tendency to experience negative affection, such as anxiety, worry, fear, anger, frustration, envy, jealousy, guilt, depressive mood and loneliness, especially when threatened, frustrated, or facing loss (Thompson, 2008; for review, see Ormel et al, 2013a). Functional magnetic resonance imaging (fMRI) studies revealed the critical function of limbic system in influencing the neuroticism, such as the amygdala, the hippocampus, as well as the frontal regions, e.g., the anterior cingulate cortex (ACC) and medial prefrontal cortex (mPFC; Canli, 2008; Tzschoppe et al, 2013; Aghajani et al, 2014; Everaerd et al, 2015; reviewed in Servaas et al, 2013). It is possible that the inconsistence of amygdala involvement in regulating neuroticism is highly dependent on the task type: amygdala might be highly involved in emotion and stress-related tasks (e.g., Tzschoppe et al, 2013; Everaerd et al, 2015), but less involved in decision making and neutral tasks (e.g., Forbes et al, 2014; Szameitat et al, 2016)
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