Unveiling the dynamic interplay between the hub- and spoke-components of the brain's semantic system and its impact on human behaviour

The neural architecture of semantic knowledge comprises two key structures: (i) A set of widely dispersed regions, located adjacent to the sensorimotor cortices, serve as spokes that represent various modality-specific and context-dependent contents. (ii) The anterior-temporal lobe (ATL) serves as a hub that computes the nonlinear mappings required to transform modality-specific information into pan-modality, multifaceted concepts. Little is understood regarding whether neural dynamics between the hub and spokes might flexibly alter depending on the nature of a concept and how it impinges upon behaviour. Using fMRI, we demonstrate for the first time that the ATL serves as a ‘pivot’ which dynamically forms flexible long-range networks with cortical modules specialised for different domains (in the present case, the knowledge about actions and places). In two experiments, we manipulated semantic congruity and asked participants to recognise visually presented items. In Experiment 1 (dual-object displays), the ATL increased its functional coupling with the bilateral frontoparietal action-sensitive system when the objects formed a pair that permitted semantically meaningful action. In Experiment 2 (objects embedded in a scene), the ATL augmented its coupling with the retrosplenial cortex of the place-sensitive system when the objects and scene formed a semantically coherent ensemble. Causative connectivity revealed that, while communication between the hub and spokes was bidirectional, the hub's directional impact on spokes dwarfed the strength of the inverse spoke-to-hub connectivity. Furthermore, the size of behavioural congruity effects co-varied with the strength of neural coupling between the ATL hub and action- / place-related spokes, evident both at the within-individual level (the behavioural fluctuation across scanning runs) and between-individual level (the behavioural variation of between participants). Together, these findings have important implications for understanding the machinery that links neural dynamics with semantic cognition.