Distinct roles for the anterior temporal lobe and angular gyrus in the spatiotemporal cortical semantic network

Abstract

It is now well recognised that human semantic knowledge is supported by a large neural network distributed over multiple brain regions, but the dynamic organisation of this network remains unknown. Some studies have proposed that a central semantic hub coordinates this network. We explored the possibility of different types of semantic hubs; namely “representational hubs”, whose neural activity is modulated by semantic variables, and “connectivity hubs”, whose connectivity to distributed areas is modulated by semantic variables. We utilised the spatio-temporal resolution of source-estimated Electro-/Magnetoencephalography data in a word-concreteness task (17 participants, 12 female) in order to: (i) find representational hubs at different timepoints based on semantic modulation of evoked brain activity in source space; (ii) identify connectivity hubs among left Anterior Temporal Lobe (ATL), Angular Gyrus (AG), Middle Temporal Gyrus and Inferior Frontal Gyrus based on their functional connectivity to the whole cortex, in particular sensory-motor-limbic systems; and (iii) explicitly compare network models with and without an intermediate hub linking sensory input to other candidate hub regions using Dynamic Causal Modelling (DCM) of evoked responses. ATL’s activity was modulated as early as 150ms post-stimulus, while both ATL and AG showed modulations of functional connectivity with sensory-motor-limbic areas from 150-450ms. DCM favoured models with one intermediate hub, namely ATL in an early time window and AG in a later time-window. Our results support ATL as a single representational hub with an early onset, but suggest that both ATL and AG function as connectivity hubs depending on the stage of semantic processing.