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 specialization in function, with the left ATL contributing preferentially to verbal semantic processing. We investigated the cognitive correlates of this organization, using resting-state functional connectivity as a measure of functional segregation between ATLs. We analyzed 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, nonsemantic cognition, or face recognition. Our results suggest that hemispheric specialization in the ATLs is not an innate property but rather emerges as people develop highly detailed verbal semantic representations. We speculate that this effect is a consequence of the left ATL's greater connectivity with left-lateralized written word recognition regions, which causes it to preferentially represent meaning for advanced vocabulary acquired primarily through reading.

Keywords: anterior temporal lobe; knowledge representation; resting-state functional connectivity; semantic cognition.

Fig. 1

(A) Example items from each task in our dataset and (B) seed ROIs of left and right vATLs and IFGs and their MNI coordinates.

Fig. 2

Results of linear regression models for age effects. This figure shows the modeled effects of age on RSFC between each pair of seed ROIs in each task. Shadow areas and error bars indicate 95% confidence intervals. The asterisks indicate significance level after FDR correction within dataset (i.e. 4 times for each dataset), # P = 0.070, * P < 0.05, ** P < 0.01, *** P < 0.001.

Fig. 3

Results of linear regression models for our dataset. This figure shows the modeled effects of age group and task performance on RSFC between each pair of seed ROIs. The FD covariate effects were not shown for simplicity. Shadow areas and error bars indicate 95% confidence intervals. The asterisks indicate significance level after FDR correction within each task (i.e. 8 times for each task), * P < 0.05, ** P < 0.01, *** P < 0.001.

Fig. 4

Results of linear regression model analysis for Cam-CAN dataset. This figure shows the modeled effects of age and task performance on RSFC between each pair of seed ROIs. The FD covariate effects were not shown for simplicity. Age × performance interaction is illustrated by plotting performance effects at the mean age and plus/minus 1 SD. Shadow areas and error bars indicate 95% confidence intervals. The asterisks indicate significance level after FDR correction within each task (i.e. 8 times for each task), * P < 0.05, ** P < 0.01, *** P < 0.001.