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 recombination of concepts (woman, dog, chased) enables the representation of novel events, and is thus a central feature of intelligence. Here, we use functional magnetic resonance (fMRI) and encoding models to delineate the contributions of three brain regions to the representation of relational combinations. We identify a region of anterior-medial prefrontal cortex (amPFC) that shares representations of noun-verb conjunctions across sentences: for example, a combination of "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 events sharing narrow conjunctions as dissimilar. The success of the hippocampal conjunctive encoding model is anti-correlated with generalization performance in amPFC on a trial-by-trial basis, consistent with a pattern separation mechanism. Thus, these three regions appear to play distinct, but complementary, roles in encoding compositional event structure.