Two Ways to Build a Thought: Distinct Forms of Compositional Semantic Representation Across Brain Regions

To understand a simple sentence such as “the woman chased the dog”, the human mind must dynamically organize the relevant concepts to represent who did what to whom. This structured re-combination of concepts (woman, dog, chased) enables the representation of novel events, and is thus a central feature of intelligence. Here, we use fMRI and encoding models to delineate the contributions of three brain regions to the representation of structured, relational combinations. We identify a region of rostral-medial prefrontal cortex (rmPFC) that shares representations of noun-verb conjunctions across sentences: for example, combining “woman” and “chased” to encode woman-as-chaser, distinct from woman-as-chasee. This PFC region differs from the left-mid superior temporal cortex (lmSTC) and hippocampus, two regions previously implicated in representing relations. lmSTC represents broad role combinations that are shared across verbs (e.g., woman-as-agent), rather than narrow roles, limited to specific actions (woman-as-chaser). By contrast, a hippocampal sub-region represents instances of recurring noun-verb conjunctions as dissimilar to one another, and is anti-correlated with rMPFC on a trial-by-trial basis, consistent with a pattern separation mechanism. These three regions appear to play distinct, but complementary, roles in encoding compositional event structure.