Multilayer Network Modelling of the Human Reading System

Abstract

Reading is supported by rapid and flexible coordination of neural activity across distributed brain regions. We have previously shown that left fusiform gyrus (FusG) provides a bridge flexibly linking the visual form analysis required for reading with the language system. Here, we investigate the dynamic organisation of an extending reading network encompassing classical perisylvian language areas and FusG. We do so by applying multilayer network modelling to language fMRI data acquired through the Australian Epilepsy Project, using a paradigm that contrasts reading with visuospatial judgements. The dataset included 201 participants with left dominant language, both with and without seizure disorders. We hypothesised that the relative strength of dynamic inter-actions within this extended language network is associated with reading ability. Time resolved functional connectivity was estimated using a sliding window Pearsons correlation approach, and the resulting connectivity matrices were entered into a multilayer community detection algorithm to quantify spatiotemporal community structure within the reading network. We concentrate our analyses on allegiance, the probability that a pair of regions is assigned to the same community over time. Our results show that community structure within the reading network is characterised by a preference for within hemisphere assignment over cross hemisphere assignment, as well as higher nodal allegiance among left language regions compared with their right hemisphere homologues. As anticipated, within versus between network allegiance followed a similar gradient in both language and attention networks: lowest between left language and right attentional regions, intermediate between the left FusG and each respective network, and highest within-network (left language or right attention). Importantly, as hypothesised, reading ability was associated with FusG-inferior frontal gyrus (IFG) interactions: higher left FusG-left IFG allegiance correlated with better reading performance, whereas increased right FusG-left IFG allegiance correlated with poorer reading. These findings highlight hemispheric asymmetries in the dynamic organisation of the reading system and provide novel evidence linking individual differences in reading ability to network level dynamics. Our findings align with a developmental literature suggesting that as reading proficiency improves, there is a shift from bilateral to unilateral left occipitotemporal engagement.