Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection

Abstract

Analyses of functional interactions between large-scale brain networks have identified two broad systems that operate in apparent competition or antagonism with each other. One system, termed the default mode network (DMN), is thought to support internally oriented processing. The other system acts as a generic external attention system (EAS) and mediates attention to exogenous stimuli. Reports that the DMN and EAS show anticorrelated activity across a range of experimental paradigms suggest that competition between these systems supports adaptive behavior. Here, we used functional MRI to characterize functional interactions between the DMN and different EAS components during performance of a recollection task known to coactivate regions of both networks. Using methods to isolate task-related, context-dependent changes in functional connectivity between these systems, we show that increased cooperation between the DMN and a specific right-lateralized frontoparietal component of the EAS is associated with more rapid memory recollection. We also show that these cooperative dynamics are facilitated by a dynamic reconfiguration of the functional architecture of the DMN into core and transitional modules, with the latter serving to enhance integration with frontoparietal regions. In particular, the right posterior cingulate cortex may act as a critical information-processing hub that provokes these context-dependent reconfigurations from an intrinsic or default state of antagonism. Our findings highlight the dynamic, context-dependent nature of large-scale brain dynamics and shed light on their contribution to individual differences in behavior.

Fig. 1.

Connectivity Z maps and sample mean network time courses of each of the five networks of interest. Dotted lines represent SD. Time courses are overlaid on a task regressor modeling activity associated with recollection blocks and indicating the onset of these trials relative to the baseline condition (gray line, arbitrary units). The spatial maps display voxels showing significant functional connectivity at P < 0.05, familywise error corrected (cluster extent > 10 voxels). Left hemisphere presented on the right hand side of each panel.

Fig. 2.

Illustration of node-specific functional roles mediating task-related and task-unrelated functional interactions between the DMN and RFPN. (A) Anatomical location of spherical regions of interest that comprise the DMN (magenta) and RFPN (green) modules, as identified by the modular decomposition of the task-unrelated functional connectivity data (maps colored according to the original assignments implied by the ICA can be seen in Fig. S5). (B) Task-unrelated group consistency coclassification matrices (SI Text, section S.5) reordered to emphasize the optimal modular structure for the sample. Solid black lines indicate boundaries between modules. Arrows highlight regions with module assignment that differed from the assignment implied by the initial ICA. (C) Fruchterman–Reingold force-directed projections showing intra- and intermodular connectivity in the task-unrelated network. Strongly connected nodes are placed in closer proximity to each other. Intramodule connections are colored according to the module identity of the nodes that they interconnect. Intermodular connections are colored black. Yellow arrows highlight regions with module assignments that differ from the assignments implied by the initial ICA (Fig. S5). (D) Scatterplots of classification consistency, z, and classification diversity, h, of each region in the task-unrelated data. Colors indicate the module to which each region belongs. (E) Location of regions belonging to the RFPN (green), DMNa (magenta), and DMNb (cyan) modules identified in the task-related functional connectivity analysis. (F–H) Group coclassification matrix, force-directed projection, and consistency-diversity scatterplot, respectively, for the task-related data. Table S2 explains the abbreviated node labels. R, right hemisphere; L, left hemisphere.