Abstract
How do large-scale brain networks reorganize during the waxing and waning of anxious anticipation? Here, threat was dynamically modulated during human functional MRI as two circles slowly meandered on the screen; if they touched, an unpleasant shock was delivered. We employed intersubject correlation analysis, which allowed the investigation of network-level functional connectivity across brains, and sought to determine how network connectivity changed during periods of approach (circles moving closer) and periods of retreat (circles moving apart). Analysis of positive connection weights revealed that dynamic threat altered connectivity within and between the salience, executive, and task-negative networks. For example, dynamic functional connectivity increased within the salience network during approach and decreased during retreat. The opposite pattern was found for the functional connectivity between the salience and task-negative networks: decreases during approach and increases during approach. Functional connections between subcortical regions and the salience network also changed dynamically during approach and retreat periods. Subcortical regions exhibiting such changes included the putative periaqueductal gray, putative habenula, and putative bed nucleus of the stria terminalis. Additional analysis of negative functional connections revealed dynamic changes, too. For example, negative weights within the salience network decreased during approach and increased during retreat, opposite what was found for positive weights. Together, our findings unraveled dynamic features of functional connectivity of large-scale networks and subcortical regions across participants while threat levels varied continuously, and demonstrate the potential of characterizing emotional processing at the level of dynamic networks.
Highlights
Imagine yourself reclining on a dentist’s chair
How do functional connectivity properties of large-scale networks evolve during periods of threat approach and retreat? During dynamic threat, what is the relationship between cortical and subcortical regions important for threat processing? We investigated functional connectivity based on intersubject correlation analysis (Hasson et al, 2004), where time series data from voxels/regions of interest (ROIs) are correlated across participants (Figure 2A)
We focused on regions of the salience, executive, and task-negative networks, as well as a targeted set of subcortical ROIs
Summary
Most of us wait anxiously as the dentist gradually moves the drill toward our mouth. If the drill is moved away (perhaps the dentist needed an additional adjustment), anxious apprehension likely will subside. A growing literature of both non-human and human research indicates that anticipatory processing of negative events engages multiple brain regions (Davis et al, 2010; Grupe and Nitschke, 2013; Tovote et al, 2015), including medial prefrontal cortex, insula, and orbitofrontal cortex, cortically. Aberrant responding to uncertain future negative events is believed to be central to anxiety disorders (Grupe and Nitschke, 2013; Fox and Kalin, 2014). Further elucidation of the mechanisms of anticipatory processing is important from both basic and clinical perspectives
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