Network analysis reveals increased integration during emotional and motivational processing

Abstract

In recent years, a large number of human studies have investigated large-scale network properties of the brain, typically during the resting state. A critical gap in the knowledge base concerns the understanding of network properties of a focused set of brain regions during task conditions engaging these regions. Although emotion and motivation recruit many brain regions, it is currently unknown how they affect network-level properties of inter-region interactions. In the present study, we sought to characterize network structure during "mini-states" engendered by emotional and motivational cues investigated in separate studies. To do so, we used graph-theoretic network analysis to probe network-, community-, and node-level properties of the trial-by-trial functional connectivity between regions of interest. We used methods that operate on weighted graphs that make use of the continuous information of connectivity strength. In both the emotion and motivation datasets, global efficiency increased and decomposability decreased. Thus, processing became less segregated with the context signaled by the cue (potential shock or potential reward). Our findings also revealed several important features of inter-community communication, including notable contributions of the bed nucleus of the stria terminalis, anterior insula, and thalamus during threat and of the caudate and nucleus accumbens during reward. Together, the results suggest that one way in which emotional and motivational processing affect brain responses is by enhancing signal communication between regions, especially between cortical and subcortical ones.

Figure 1.

Experimental paradigms. In both tasks, an initial cue signaled the trial condition: safe and threat in the emotion study, and control and reward in the motivation study. A, Subjects performed a response–conflict task under two contexts, safe and threat. During the threat condition (shown here), a cue stimulus (diamond) signaled that a mild electric shock could occur during the delay period after cue offset and before the target display (independently of task performance). During the subsequent target phase, participants were asked to indicate whether the picture contained a house or a building, while ignoring the superimposed word. During the safe condition (data not shown), the trial structure was identical, except for the shape of the cue stimulus (rectangle) and the fact that shocks were never administered during the delay period. B, Subjects performed a response–conflict task under two contexts, control and reward. During the reward condition (shown here), a cue stimulus (“$20”) signaled that participants would be rewarded for fast and correct performance; during the control condition (not shown here), a cue stimulus (“$00”) signaled that no reward was involved. During the subsequent target phase, participants were asked to indicate whether the picture contained a house or a building, while ignoring the superimposed word. After the target stimulus, subjects were informed about the potential reward and about the total points accrued.

Figure 2.

A, Anatomical slices showing ROIs used in the network analysis of the emotion dataset. For abbreviations, see Table 1. B, Anatomical slices showing ROIs used in the network analysis of the motivation dataset. For abbreviations, see Table 2.

Figure 3.

Force layout depiction of the group-level network in the emotion dataset during the safe condition. Nodes are colored to show community organization (red for subcortical community, teal for cortical community). Edges are also colored according to communities with between-community edges colored purple. For visualization purposes, edges were thresholded to leave only the ∼50% strongest ones. Visualization done with Gephi 0.8 beta, making use of the Force Atlas and label-adjust layout tools. For abbreviations, see Table 1.

Figure 4.

Changes in threat versus safe connectivity for the group-level network in the emotion dataset. Within-cortical connections are bounded by a teal box, and within-subcortical connections are bounded by a green box. For abbreviations, see Table 1.

Figure 5.

A, Changes in threat versus safe connectivity between communities for the group-level network in the emotion dataset. Only significant (p < 0.05, FDR corrected) changes are shown (nonsignificant connections are gray). B, Only between-community edges with significant threat versus safe connectivity changes are shown (p < 0.05, FDR corrected). Node positions and colors as in Figure 3. Visualization done with Gephi 0.8 beta, making use of the Force Atlas and label-adjust layout tools. C, Polar plots illustrating the changes of key cortical and subcortical nodes from A. Distance from the dark centered hexagon/decagon corresponds to change in connectivity (threat–safe). Nonsignificant changes were set to zero. For abbreviations, see Table 1.

Figure 6.

Force layout depiction of the group-level network in the motivation dataset during the control condition. Nodes are colored to show community organization (red for subcortical community, teal for cortical community). Edges are also colored according to communities with between-community edges colored purple. For visualization purposes, edges were thresholded to leave only the ∼40% strongest ones. Visualization done with Gephi 0.8 beta, making use of the Force Atlas and label adjust-layout tools. For abbreviations, see Table 2.

Figure 7.

Changes in reward versus control connectivity for the group-level network in the motivation dataset. Within-cortical connections are bounded by a teal box, and within-subcortical edges are bounded by a green box. For abbreviations, see Table 2.

Figure 8.

A, Change in reward versus control connectivity between communities for the group-level network in the motivation dataset. Only significant (p < 0.05, FDR corrected) changes are shown (nonsignificant connections are gray). B, Only between-community edges with significant reward versus control connectivity changes are shown (p < 0.05, FDR corrected). Node positions and colors as in Figure 6. Visualization done with Gephi 0.8 beta, making use of the Force Atlas and label-adjust layout tools. C, Polar plots illustrating three key subcortical nodes from A. Distance from the dark centered polygon corresponds to change in connectivity (reward–control). Nonsignificant changes were set to zero. For abbreviations, see Table 2.