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. 2010 Oct 15;53(1):303-17.
doi: 10.1016/j.neuroimage.2010.06.016. Epub 2010 Jun 18.

Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition

R Nathan Spreng  1 , W Dale Stevens, Jon P Chamberlain, Adrian W Gilmore, Daniel L Schacter
Affiliations

Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition

R Nathan Spreng et al. Neuroimage. .

Abstract

Tasks that demand externalized attention reliably suppress default network activity while activating the dorsal attention network. These networks have an intrinsic competitive relationship; activation of one suppresses activity of the other. Consequently, many assume that default network activity is suppressed during goal-directed cognition. We challenge this assumption in an fMRI study of planning. Recent studies link default network activity with internally focused cognition, such as imagining personal future events, suggesting a role in autobiographical planning. However, it is unclear how goal-directed cognition with an internal focus is mediated by these opposing networks. A third anatomically interposed 'frontoparietal control network' might mediate planning across domains, flexibly coupling with either the default or dorsal attention network in support of internally versus externally focused goal-directed cognition, respectively. We tested this hypothesis by analyzing brain activity during autobiographical versus visuospatial planning. Autobiographical planning engaged the default network, whereas visuospatial planning engaged the dorsal attention network, consistent with the anti-correlated domains of internalized and externalized cognition. Critically, both planning tasks engaged the frontoparietal control network. Task-related activation of these three networks was anatomically consistent with independently defined resting-state functional connectivity MRI maps. Task-related functional connectivity analyses demonstrate that the default network can be involved in goal-directed cognition when its activity is coupled with the frontoparietal control network. Additionally, the frontoparietal control network may flexibly couple with the default and dorsal attention networks according to task domain, serving as a cortical mediator linking the two networks in support of goal-directed cognitive processes.

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Figures

Figure 1
Figure 1
Task Stimuli. For the visuospatial planning condition, participants performed the Tower of London task. In this condition participants saw the goal configuration for 5 seconds, then the start configuration for a maximum of 15 seconds, and determined the minimum number of moves to match the start with the goal configuration. Participants then indicated the minimum number of moves to solve the puzzle. In the autobiographical planning task condition, participants were presented with a goal state, followed by a combination of two steps and an obstacle related to that goal printed in the discs. Participants integrated the steps and obstacle into an authentic and coherent personal plan to reach that goal. In this example, participants interpreted the goal state “Freedom from Debt” for 5 seconds. For up to 15 seconds, participants integrated the steps “Good job”, “Save Money” as well as the obstacle “Have Fun” into a plan to be free of debt. Next, participants rated the level of detail in their plan. In the Count condition, participants were informed they would count vowels, then random letter sequences appeared in the discs. Next, participants indicated the number of vowels counted. If participants completed any of the tasks prior to 15 seconds, a button was pressed and the screen advanced to the rating screen. Remaining time was added to the inter-trial interval.
Figure 2
Figure 2
Task-related brain activity in default and dorsal attention networks dissociated the planning tasks. (A) Activity associated with autobiographical planning (Blue) and visuospatial planning (Red) at TR 6 (17.5 s). Real-time patterns of activation at each TR associated with planning are available as Supplemental Movies 1 and 2. Data are displayed on the dorsal, lateral, medial, and ventral surfaces of the left and right hemispheres of a partially inflated surface map using CARET software (Van Essen, 2005). (B) Design scores for each condition represent the optimal contrast weightings that explain the most task-related variance in BOLD signal. Autobiographical planning was maximally dissociated from visuospatial planning. Counting activity covaried across the same regions as visuospatial planning, although significantly less so. (C) Temporal brain scores convey changes in brain activity related to task at each TR. For each LV, mean brain scores (summary scores of activity across the entire brain of each participant, averaged across participants) show the divergence between experimental conditions over time (Ten 2.5s TRs), and are analogous to hemodynamic response functions typically plotted for individual brain regions.
Figure 3
Figure 3
Task-related brain activity in frontoparietal control network is common to both planning tasks. (A) Activity associated with both planning tasks (Green) at TR 6 (17.5 s). The design scores (B) and temporal brain scores (C) dissociate both autobiographical and visuospatial planning from counting. Real-time patterns of activation at each TR associated with planning are available as Supplemental Movies 1 and 2.
Figure 4
Figure 4
Resting-state functional connectivity analysis. Seed regions used to compute the correlation maps are shown to the left of the (A) default, (B) dorsal attention, and (C) frontoparietal control resting-state networks. Task salience is a measure of task-based activity in each resting-state network ROI. Y-axis = extracted mean voxel-salience (10−4) within each ROI from the first latent variable for the autobiographical and visuospatial planning tasks, and from the second latent variable for the conjunction of both planning tasks relative to counting. Task salience values quantitatively demonstrate that (A) the default network was primarily engaged by autobiographical planning, (B) the dorsal attention network was primarily engaged by visuospatial planning and, (C) the frontoparietal control network was primarily engaged by activity underlying both planning tasks. HF = Hippocampal formation; AB Plan = autobiographical planning; VS Plan = visuospatial planning; AB & VS Plan = activity common to both planning tasks.
Figure 5
Figure 5
Lateral parietal view of the PLS and rsfcMRI results. Left parietal lobe activity for autobiographical planning, visuospatial planning and activity common to these two planning tasks (left); and the default, dorsal attention, and frontoparietal control resting-state networks (right). (A) pIPL activity in autobiographical planning subsumes the pIPL cluster in the default resting-state network. (B) Visuospatial planning engaged the same SPL-to-MT+ arc seen in the posterior portion of the dorsal attention network. (C) The two planning tasks commonly engaged a dorsal segment of the aIPL, part of the frontoparietal control network. (D) Overlap of all three networks for task-related activity and resting-state networks. Yellow represents overlap. The cluster ventral to the aIPL in the posterior middle temporal gyrus is suggestive of a concentric ring fitting within the posterior arc of the dorsal attention network. The pIPL region associated with the default network fills this ring. The rsfcMRI results do not mirror this concentric ring pattern, suggesting that it may be task specific. See also Supplemental Fig. 3 for whole brain convergence images of task activity and resting-state network maps.
Figure 6
Figure 6
Mean and SEM of planning task-related percent BOLD signal change within each resting-state network. (A) Default network. (B) Dorsal attention network. (C) Frontoparietal control network. * indicates significant task difference in BOLD signal from baseline.
Figure 7
Figure 7
Frontoparietal control network coupling modulated by task. The frontoparietal control network is reliably correlated with the default network during autobiographical planning, but not during visuospatial planning, across the trial interval (2.5 – 25.0 seconds). The dorsal attention network is reliably correlated with the frontoparietal control network during visuospatial planning, but not during autobiographical planning.
Figure 8
Figure 8
Task-related Functional Connectivity Analysis. Seed PLS results illustrate regions that are functionally connected with the default network ROI BOLD value during autobiographical planning, and with the dorsal attention network ROI BOLD value during visuospatial planning. All three conditions for network coupling were met. During autobiographical planning, network coupling between the default and frontoparietal control networks were demonstrated by A) Default seed network autocorrelations (depicted on the medial surface), B) Default network seed connectivity with the frontoparietal control network (depicted on an anterior view of the prefrontal lobes) and C) a relative absence of connectivity with the dorsal attention network (depicted on a lateral posterior surface). During visuospatial planning, network coupling between the dorsal attention and frontoparietal control networks were demonstrated by D) Dorsal attention seed network autocorrelations (lateral posterior), E) Dorsal attention network seed connectivity with the frontoparietal control network (anterior) and F) a relative absence of connectivity with the default network (medial). Outlined regions are the rsfcMRI maps: Blue = Default network on the medial surface, Red = Dorsal attention network on the lateral posterior surface, Green = Frontoparietal control network on the anterior frontal lobes. Images are thresholded at p < .001 (PLS identifies whole brain patterns of activity in a single analytic step, thus, no correction for multiple comparisons is required). See Supplemental Figure 5 for whole brain results. AB Plan = autobiographical planning; VS Plan = visuospatial planning; R = right; L = left.
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