Overlapping connectivity gradients in the anterior temporal lobe underlie semantic cognition

Abstract

Convergent evidence from neuroimaging, computational, and clinical research has shown that the anterior temporal lobe (ATL) is critically involved in two key aspects of semantic cognition: the representation of semantic knowledge, and the executive regulation of this knowledge. Both are necessary for integrating features to understand concepts, and to integrate concepts to understand discourse. Here, we tested the hypothesis that these differential aspects of integration map onto different patterns of ATL connectivity. Specifically, we hypothesized that there are two overlapping modes of functional connectivity of the ATL that each predict distinct aspects of semantic cognition on an individual level. We used a novel analytical approach (connectopic mapping) to identify the first two dominant modes connection topographies (i.e. maps of spatially varying connectivity) in the ATL in 766 participants (Human Connectome Project), and summarized these into 16 parameters that reflect inter-individual differences in their functional organization. If these connection topographies reflect the ATLs functional multiplicity, then we would expect to find a dissociation where one mode (but not the other) correlates with cross-modal matching of verbal and visual information (picture vocabulary naming), and the other (but not the former) correlates with how quickly and accurately relevant semantic information is retrieved (story comprehension). Our analysis revealed a gradient of spatially varying connectivity along the inferior-superior axis, and secondly, an anterior to posterior gradient. Multiple regression analyses revealed a double dissociation such that individual differences in the inferior-superior gradient are predictive of differences in story comprehension, whereas the anterior-posterior gradient maps onto differences in picture vocabulary naming, but not vice versa. These findings indicate that overlapping gradients of functional connectivity in the ATL are related to differential behaviors, which is important for understanding how its functional organization underlies its multiple functions.