Verbal semantic expertise is associated with reduced functional connectivity between left and right anterior temporal lobes

Abstract

The left and right anterior temporal lobes (ATLs) encode semantic representations. They show graded hemispheric specialisation in function, with the left ATL contributing preferentially to verbal semantic processing. We investigated the underlying causes of this organisation, using resting-state functional connectivity as a measure of functional segregation between ATLs. We analysed two independent resting-state fMRI datasets (N=86 and N=642) in which participants verbal semantic expertise was measured using vocabulary tests. In both datasets, people with more advanced verbal semantic knowledge showed weaker functional connectivity between left and right ventral ATLs. This effect was highly specific. It was not observed for within-hemisphere connections between semantic regions (ventral ATL and inferior frontal gyrus; IFG, though it was found for left-right IFG connectivity in one dataset). Effects were not found for tasks probing semantic control, non-semantic cognition or face recognition. Our results suggest that hemispheric specialisation in the ATLs is not an innate property but rather emerges as people develop highly detailed verbal semantic representations. We propose that this effect is a consequence of the left ATLs greater connectivity with left-lateralised written word recognition regions, which causes it to preferentially represent meaning for advanced vocabulary acquired primarily through reading.