Abstract
Semantic knowledge is supported by numerous brain regions, but the spatiotemporal configuration of the network that links these areas remains an open question. The hub-and-spokes model posits that a central semantic hub coordinates this network. In this study, we explored distinct aspects that define a semantic hub, as reflected in the spatiotemporal modulation of neural activity and connectivity by semantic variables, from the earliest stages of semantic processing. We used source-reconstructed electro/magnetoencephalography, and investigated the concreteness contrast across three tasks. In a whole-cortex analysis, the left anterior temporal lobe (ATL) was the only area that showed modulation of evoked brain activity from 100 ms post-stimulus. Furthermore, using Dynamic Causal Modeling of the evoked responses, we investigated effective connectivity amongst the candidate semantic hub regions, that is, left ATL, supramarginal/angular gyrus (SMG/AG), middle temporal gyrus, and inferior frontal gyrus. We found that models with a single semantic hub showed the highest Bayesian evidence, and the hub region was found to change from ATL (within 250 ms) to SMG/AG (within 450 ms) over time. Our results support a single semantic hub view, with ATL showing sustained modulation of neural activity by semantics, and both ATL and AG underlying connectivity depending on the stage of semantic processing.
Highlights
When we see a word, how do we understand its meaning? What areas in the brain are involved and how do these areas connect over time to form the neuronal networks that support retrieval of semantic knowledge? Ample evidence, predominantly based on neuropsychology and functional magnetic resonance imaging (Binder et al 2009; Lambon Ralph et al 2016), points to the involvement of a large number of brain regions in semantic processing, in the left hemispheric temporal, parietal, and frontal regions (Binder and Desai 2011)
Using Dynamic Causal Modeling of the evoked responses, we investigated effective connectivity amongst the candidate semantic hub regions, that is, left anterior temporal lobe (ATL), supramarginal/angular gyrus (SMG/AG), middle temporal gyrus, and inferior frontal gyrus
We found that models with a single semantic hub showed the highest Bayesian evidence, and the hub region was found to change from ATL to Supramarginal Gyrus (SMG)/AG over time
Summary
When we see a word, how do we understand its meaning? What areas in the brain are involved and how do these areas connect over time to form the neuronal networks that support retrieval of semantic knowledge? Ample evidence, predominantly based on neuropsychology and functional magnetic resonance imaging (fMRI) (Binder et al 2009; Lambon Ralph et al 2016), points to the involvement of a large number of brain regions in semantic processing, in the left hemispheric temporal, parietal, and frontal regions (Binder and Desai 2011). One of the most prominent models of semantic processing is the hub-and-spokes model (Patterson et al 2007), which proposes that a single hub region in the anterior temporal lobe (ATL) binds the semantic network together (Rogers et al 2004; Lambon Ralph et al 2016) Strong evidence for this model has come from computational modeling (Rogers et al 2004; Chen et al 2017; Hoffman et al 2018), neuroimaging research (Lau et al 2013; Binney et al 2016; Jackson et al 2016; Lambon Ralph et al 2016), and from studies on semantic dementia, a type of neurodegenerative brain disorder that is associated with damage to the ATLs and a profound loss of semantic knowledge (Snowden et al 1989, 2017; Rogers et al 2004; Patterson et al 2007). A prominent alternative model is the theory of convergence zones (Barsalou 2009; Meyer and Damasio 2009; Martin 2016), where multiple heteromodal regions, for example, in the posterior inferior parietal lobe
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