A Heteromodal Word-Meaning Binding Site in the Visual Word Form Area under Top-Down Frontoparietal Control

The integral capacity of human language together with semantic memory drives the linkage of words and their meaning, which theoretically is subject to cognitive control. However, it remains unknown whether, across different language modalities and input/output formats, there is a shared system in the human brain for word-meaning binding and how this system interacts with cognitive control. Here, we conducted a functional magnetic resonance imaging experiment based on a large cohort of subjects (50 females, 50 males) to comprehensively measure the brain responses evoked by semantic processing in spoken and written word comprehension and production tasks (listening, speaking, reading, and writing). We found that heteromodal word input and output tasks involved distributed brain regions within a frontal-parietal-temporal network and focally coactivated the anterior lateral visual word form area (VWFA), which is located in the basal occipitotemporal area. Directed connectivity analysis revealed that the VWFA was invariably under significant top-down modulation of the frontoparietal control network and interacts with regions related to attention and semantic representation. This study reveals that the VWFA is a key site subserving general semantic processes linking words and meaning, challenging the predominant emphasis on this area's specific role in reading or more general visual processes. Our findings also suggest that the dynamics between semantic memory and cognitive control mechanisms during word processing are largely independent of the modalities of input or output.SIGNIFICANCE STATEMENT Binding words and their meaning into a coherent whole during retrieval requires accessing semantic memory and cognitive control, allowing our thoughts to be expressed and comprehended through mind-external tokens in multiple modalities, such as written or spoken forms. However, it is still unknown whether multimodal language comprehension and production share a common word-meaning binding system in human brains and how this system is connected to a cognitive control mechanism. By systematically measuring brain activity evoked by spoken and written verbal input and output tasks tagging word-meaning binding processes, we demonstrate a general word-meaning binding site within the visual word form area (VWFA) and how this site is modulated by the frontal-parietal control network.