Distinctive and complementary roles of default mode network subsystems in semantic cognition

The default mode network (DMN) typically deactivates to external tasks, yet supports semantic cognition. It comprises medial temporal (MT), core, and fronto-temporal (FT) subsystems, but its functional organisation is unclear: the requirement for perceptual coupling versus decoupling, input modality (visual/verbal), type of information (social/spatial) and control demands all potentially affect its recruitment. We examined the effect of these factors on activation and deactivation of DMN subsystems during semantic cognition, across four task-based functional magnetic resonance imaging (fMRI) datasets, and localised these responses in whole-brain state space defined by gradients of intrinsic connectivity. FT showed activation consistent with a central role across domains, tasks and modalities, although it was most responsive to abstract, verbal tasks; this subsystem uniquely showed more ‘tuned’ states characterised by increases in both activation and deactivation when semantic retrieval demands were higher. MT also activated to both perceptually-coupled (scenes) and decoupled (autobiographical memory) tasks, and showed stronger responses to picture associations, consistent with a role in scene construction. Core DMN consistently showed deactivation, especially to externally-oriented tasks. These diverse contributions of DMN subsystems to semantic cognition were related to their location on intrinsic connectivity gradients: activation was closer to sensory-motor cortex than deactivation, particularly for FT and MT, while activation for core DMN was distant from both visual cortex and cognitive control. These results reveal distinctive yet complementary DMN responses: MT and FT support different memory-based representations that are accessed externally and internally, while deactivation in core DMN is associated with demanding, external semantic tasks. Significance Statement We delineate the functional organisation of DMN in semantic cognition, examining effects of perceptual coupling versus decoupling, input modality (visual/verbal), domain (social/spatial) and control demands across DMN subsystems in four fMRI datasets. These subsystems played complementary roles in semantic cognition related to their locations on gradients of intrinsic connectivity. Medial temporal and frontotemporal subsystems supported visuospatial and abstract conceptual information respectively, across both internally and externally-focussed tasks, while deactivation in core DMN was associated with focussed and externally-oriented semantic states. We conclude that both content and process are relevant to the functional architecture of DMN in semantic cognition.