The White Matter Module-Hub Network of Semantics Revealed by Semantic Dementia

Abstract

Cognitive neuroscience exploring the architecture of semantics has shown that coherent supramodal concepts are computed in the anterior temporal lobes (ATL), but it is unknown how/where modular information implemented by posterior cortices (word/object/face forms) is conveyed to the ATL hub. We investigated the semantic module-hub network in healthy adults (n = 19) and in semantic dementia patients (n = 28) by combining semantic assessments of verbal and nonverbal stimuli and MRI-based fiber tracking using seeds in three module-related cortices implementing (i) written word forms (visual word form area), (ii) abstract lexical representations (posterior–superior temporal cortices), and (iii) face/object representations (face form area). Fiber tracking revealed three key tracts linking the ATL with the three module-related cortices. Correlation analyses between tract parameters and semantic scores indicated that the three tracts subserve semantics, transferring modular verbal or nonverbal object/face information to the left and right ATL, respectively. The module-hub tracts were functionally and microstructurally damaged in semantic dementia, whereas damage to non-module-specific ATL tracts (inferior longitudinal fasciculus, uncinate fasciculus) had more limited impact on semantic failure. These findings identify major components of the white matter module-hub network of semantics, and they corroborate/materialize claims of cognitive models positing direct links between modular and semantic representations. In combination with modular accounts of cognition, they also suggest that the currently prevailing “hub-and-spokes” model of semantics could be extended by incorporating an intermediate module level containing invariant representations, in addition to “spokes,” which subserve the processing of a near-unlimited number of sensorimotor and speech-sound features.