An architecture for encoding sentence meaning in left mid-superior temporal cortex

Significance The 18th-century Prussian philosopher Wilhelm von Humbolt famously noted that natural language makes “infinite use of finite means.” By this, he meant that language deploys a finite set of words to express an effectively infinite set of ideas. As the seat of both language and thought, the human brain must be capable of rapidly encoding the multitude of thoughts that a sentence could convey. How does this work? Here, we find evidence supporting a long-standing conjecture of cognitive science: that the human brain encodes the meanings of simple sentences much like a computer, with distinct neural populations representing answers to basic questions of meaning such as “Who did it?” and “To whom was it done?” Human brains flexibly combine the meanings of words to compose structured thoughts. For example, by combining the meanings of “bite,” “dog,” and “man,” we can think about a dog biting a man, or a man biting a dog. Here, in two functional magnetic resonance imaging (fMRI) experiments using multivoxel pattern analysis (MVPA), we identify a region of left mid-superior temporal cortex (lmSTC) that flexibly encodes “who did what to whom” in visually presented sentences. We find that lmSTC represents the current values of abstract semantic variables (“Who did it?” and “To whom was it done?”) in distinct subregions. Experiment 1 first identifies a broad region of lmSTC whose activity patterns (i) facilitate decoding of structure-dependent sentence meaning (“Who did what to whom?”) and (ii) predict affect-related amygdala responses that depend on this information (e.g., “the baby kicked the grandfather” vs. “the grandfather kicked the baby”). Experiment 2 then identifies distinct, but neighboring, subregions of lmSTC whose activity patterns carry information about the identity of the current “agent” (“Who did it?”) and the current “patient” (“To whom was it done?”). These neighboring subregions lie along the upper bank of the superior temporal sulcus and the lateral bank of the superior temporal gyrus, respectively. At a high level, these regions may function like topographically defined data registers, encoding the fluctuating values of abstract semantic variables. This functional architecture, which in key respects resembles that of a classical computer, may play a critical role in enabling humans to flexibly generate complex thoughts.