Aberrant degree centrality profiles during rumination in major depressive disorder

Abstract

Rumination is closely linked to the onset and maintenance of major depressive disorder (MDD). Prior neuroimaging studies have identified the association between self-reported rumination trait and the functional coupling among a network of brain regions using resting-state functional magnetic resonance imaging (MRI). However, little is known about the underlying neural circuitry mechanism during active rumination in MDD. Degree centrality (DC) is a simple metric to denote network integration, which is critical for higher-order psychological processes such as rumination. During an MRI scan, individuals with MDD (N = 45) and healthy controls (HC, N = 46) completed a rumination state task. We examined the interaction effect between the group (MDD vs. HC) and condition (rumination vs. distraction) on vertex-wise DC. We further characterized the identified brain region's functional involvement with Neurosynth and BrainMap. Network-wise seed-based functional connectivity (FC) analysis was also conducted for the identified region of interest. Finally, exploratory correlation analysis was conducted between the identified region of interest's network FCs and self-reported in-scanner affect levels. We found that a left superior frontal gyrus (SFG) region, generally overlapped with the frontal eye field, showed a significant interaction effect. Further analysis revealed its involvement with executive functions. FCs between this region, the frontoparietal, and the dorsal attention network (DAN) also showed significant interaction effects. Furthermore, its FC to DAN during distraction showed a marginally significant negative association with in-scanner affect level at the baseline. Our results implicated an essential role of the left SFG in the rumination's underlying neural circuitry mechanism in MDD and provided novel evidence for the conceptualization of rumination in terms of impaired executive control.

Keywords: degree centrality; dorsal attention network; executive function; fMRI; major depressive disorder; rumination.

FIGURE 1

Overview of the experimental design and analytical framework. (a) MDD patients and HCs were induced to reflect on themselves (rumination) or focus on an external topic (distraction). The sequence of the rumination and distraction sessions was counterbalanced across all participants. (b) A vertex‐wised DC map was calculated, and a mixed effect analysis was performed vertex by vertex to generate a t map. DC, degree centrality; HC, healthy control; MDD, major depressive disorder.

FIGURE 2

Subjects' self‐reported mood levels and the brain region showing a significant interaction effect. (a) Violin plots showing the distributions of in‐scanner mood levels. (b) The left SFG region showing a significant interaction effect. (c) The MDD patients yielded decreased DC in the left SFG in the rumination compared with the distraction state, while the HCs showed an opposite pattern. (d) Word clouds of cognitive functions associated with the left SFG cluster. DC, degree centrality; HC, healthy control; MDD, major depressive disorder; SFG, superior frontal gyrus.

FIGURE 3

The FCs between the left SFG and the DAN and FPN showed significant interaction effects. (a) The FCs between the left SFG region and the DAN. (b) The FCs between the left SFG and the FPN. DAN, dorsal attention network; FC, functional connectivity; FPN, frontoparietal network; SFG, superior frontal gyrus.

FIGURE 4

Relationship between the baseline in‐scanner affect levels and the SFG region's network FCs. DAN, dorsal attention network; FPN, frontoparietal network; HC, healthy control; MDD, major depressive disorder.