Dynamic disconnection of the supplementary motor area after processing of dismissive biographic narratives

Abstract

Introduction: To understand the interplay between affective social information processing and its influence on mental states we investigated changes in functional connectivity (FC) patterns after audio exposure to emotional biographic narratives.

Methods: While lying in the 7T MR scanner, 23 male participants listened to narratives of early childhood experiences of three persons, each having either a secure, dismissing, or preoccupied attachment representation. Directly after having listened to each of the prototypical narratives, participants underwent a 10-minute resting-state fMRI scan. To study changes in FC patterns between experimental conditions, three post-task conditions were compared to a baseline condition. Specific local alterations, as well as differences in connectivity patterns between distributed brain regions, were quantified using Network-based statistics (NBS) and graph metrics.

Results: Using NBS, a nine-region subnetwork showing reduced FC after having listened to the dismissing narrative was identified. Of this subnetwork, only the left Supplementary Motor Area (SMA) exhibited a decrease in the nodal graph metrics degree and strength exclusively after listening to the dismissing narrative. No other region showed post-task changes in nodal metrics. A post hoc analysis of dynamic characteristics of FC of the left SMA showed a significant decrease in the dismissing condition when compared with the other conditions in the first three minutes of the scan, but faded away in the two subsequent intervals the differences.

Conclusions: Nodal metrics and NBS converge on reduced connectivity measures exclusively in left SMA in the dismissing condition, which may specifically reflect ongoing network changes underlying prolonged emotional reactivity to attachment-related processing.

Keywords: Acoustic stimulation; adult attachment representation; cognitive affective neuroscience; fMRI; functional connectivity; graph theory; human social interactions; resting‐state.

Figure 1

Course of tasks in the experimental design.

Figure 2

Depiction of the static network‐based statistics “core‐subnetwork” (consisting of 9 nodes and 9 links, threshold = 4) showing reduced connections in the resting phase after listening to the dismissing narrative when compared to the baseline resting condition. See Table 2 for node abbreviations. This visualization was created using BrainNet Viewer Toolbox (Xia et al., 2013).

Figure 3

Area‐under‐the curve (AUC) plot showing significant differences (P < 0.05, as indicated by black stars) across all tested sparsity thresholds between the dismissing condition and all other conditions in the two local graph metrics strength (left) and degree (right) in the left supplementary motor area (SMA).

Figure 4

Connectivity pattern of the left supplementary motor area (SMA) (centered yellow node). Each white node depicted in the peripheral circle corresponds to an area the left SMA functionally connects to during the baseline condition. Regions that disconnect from the left SMA in the dismissing condition are depicted with a dashed line.

Figure 5

False discovery rate corrected differences in the two local graph metrics strength (left) and degree (right) of the left supplementary motor area at a sparsity threshold of 18% between time intervals after normalization to baseline condition. ***: P < 0.001 **: P < 0.01.