Distinct fronto-temporal substrates of distributional and taxonomic similarity among words: evidence from RSA of BOLD signals.

A class of semantic theories defines concepts in terms of statistical distributions of lexical items, basing meaning on vectors of word co-occurrence frequencies. A different approach emphasizes abstract hierarchical taxonomic relationships among concepts. However, the functional relevance of these different accounts and how they capture information-encoding of lexical meaning in the brain still remains elusive. We investigated to what extent distributional and taxonomic models explained word-elicited neural responses using cross-validated representational similarity analysis (RSA) of functional magnetic resonance imaging (fMRI) and model comparisons. Our findings show that the brain encodes both types of semantic information, but in distinct cortical regions. Posterior middle temporal regions reflected lexical-semantic similarity based on hierarchical taxonomies, in coherence with the action-relatedness of specific semantic word categories. In contrast, distributional semantics best predicted the representational patterns in left inferior frontal gyrus (LIFG, BA 47). Both representations coexisted in the angular gyrus supporting semantic binding and integration. These results reveal that neuronal networks with distinct cortical distributions across higher-order association cortex encode different representational properties of word meanings. Taxonomy may shape long-term lexical-semantic representations in memory consistently with the sensorimotor details of semantic categories, whilst distributional knowledge in the LIFG (BA 47) may enable semantic combinatorics in the context of language use. Our approach helps to elucidate the nature of semantic representations essential for understanding human language.