Large-scale brain network dynamics supporting adolescent cognitive control

Abstract

Adolescence is a time when the ability to engage cognitive control is linked to crucial life outcomes. Despite a historical focus on prefrontal cortex functioning, recent evidence suggests that differences between individuals may relate to interactions between distributed brain regions that collectively form a cognitive control network (CCN). Other research points to a spatially distinct and functionally antagonistic system--the default-mode network (DMN)--which typically deactivates during performance of control tasks. This literature implies that individual differences in cognitive control are determined either by activation or functional connectivity of CCN regions, deactivation or functional connectivity of DMN regions, or some combination of both. We tested between these possibilities using a multilevel fMRI characterization of CCN and DMN dynamics, measured during performance of a cognitive control task and during a task-free resting state, in 73 human adolescents. Better cognitive control performance was associated with (1) reduced activation of CCN regions, but not deactivation of the DMN; (2) variations in task-related, but not resting-state, functional connectivity within a distributed network involving both the CCN and DMN; (3) functional segregation of core elements of these two systems; and (4) task-dependent functional integration of a set of peripheral nodes into either one network or the other in response to prevailing stimulus conditions. These results indicate that individual differences in adolescent cognitive control are not solely attributable to the functioning of any single region or network, but are instead dependent on a dynamic and context-dependent interplay between the CCN and DMN.

Keywords: adolescence; cognitive control; fMRI; functional connectivity; graph theory; modularity.

Figure 1.

The MSIT is conducted using a block design with three main conditions: resting fixation, congruent stimuli, and incongruent stimuli. A, Resting fixation is the presentation of a cross-hair. B, The congruent condition involves responding to a target number that is congruent to the finger position on a button box. C, During the incongruent condition, the finger response differs from the location of the target on screen and the target is flanked by two other numbers. D, The experimental time course is depicted as an alternating block design with interleaved 15 s resting fixation periods between each 30 s block of congruent (green, B) and incongruent (red, C) trials.

Figure 2.

Identification of ROIs from task activation and resting-state functional connectivity mapping of the CCN and DMN. A, Task maps showing CCN activations during incongruent trials of the MSIT compared with congruent trials (yellow), and DMN deactivations when incongruent trials were compared with resting-fixation blocks (blue). B, Resting-state maps showing positive (blue) and negative (yellow) functional connectivity with a posterior cingulate seed region (MNI: [0 −50 30]), representative of the DMN and CCN, respectively. C, Anatomical location of 73 seed regions drawn from the maps presented in A and B. Subcortical seed regions (i–vi) depicted below. Node labels defined in Table 1.

Figure 3.

Activation correlates of interference RT. Colored nodes denote CCN (red) and DMN (blue) where regional activation was significantly correlated (FDR corrected) with interference RT. Gray nodes denote nonsignificant correlations. Node sizes are scaled according to correlation size (larger spheres = higher correlation). Scatterplots (a–k) are displayed for all significant correlations. Node labels defined in Table 1. iIPs, inferior IPS; sIPS, superior IPS; mIPS, medial IPS; SGC, subgenual cingulate, R CAUD, right caudate.

Figure 4.

A, Interference RT is correlated with task-related functional connectivity in a distributed subnetwork of CCN (red) and DMN (blue) regions (legend, bottom right). Gray connections indicate that stronger functional connectivity was associated with higher interference RT (worse performance); white connections indicate that stronger functional connectivity was associated with lower RT (better performance).The z-dimension has been collapsed to aid visualization. B, Number of connections (degree) possessed by each node in the performance-related network. Nodes are ordered from most connections (top) to least connections (bottom), and colored according to their network of origin (red, cognitive control; blue, default mode). Node locations displayed in Figure 2. Node labels defined in Table 1.

Figure 5.

Better cognitive control ability is associated with bipartite brain functional organization. Fructherman-Reingold force-directed topological layouts of functional connectivity networks from high-performing participants during rest (A) and task (B) conditions, and from low-performing participants during rest (C) and task (D) conditions. Node color represents the modular affiliation of each region as defined by graph analytic modularity analysis (red, CCN-like module; blue, DMN-like module; purple, third, intermediary module). To assist visualization, graphs have been thresholded at 50% or greater co-classification frequency across participants. Intramodule connections are colored according to the parent module, intermodule connections are colored in gray. Scatterplots illustrate putative nodes roles in terms of classification consistency and diversity (see Materials and Methods). Brain organization in high performers was dominated by two large modules in both rest and task; low performers showed consistent evidence for three modules. Nodes in this third module showed on average higher classification diversity, pointing to variable module affiliation across subjects. Node locations displayed in Figure 2. R LO, right lateral occipital cortex; L LO left lateral occipital cortex; L pLING, left posterior lingual gyrus; R TOJ2, right temporo-occipital junction; L iCS, left inferior central sulcus; R pINS, right posterior insula cortex; L sCS, left superior central sulcus; R pPH1, right parahippocampal gyrus; SGC, subgenual cingulate cortex; R PO, right parietal operculum; R pINS, right posterior insula cortex; L SMG, left supramarginal gyrus; MD, mediodorsal thalamus; R CAUD, right caudate.