Sentence processing in anterior superior temporal cortex shows a social-emotional bias

Abstract

The anterior region of the left superior temporal gyrus/superior temporal sulcus (aSTG/STS) has been implicated in two very different cognitive functions: sentence processing and social-emotional processing. However, the vast majority of the sentence stimuli in previous reports have been of a social or social-emotional nature suggesting that sentence processing may be confounded with semantic content. To evaluate this possibility we had subjects read word lists that differed in phrase/constituent size (single words, 3-word phrases, 6-word sentences) and semantic content (social-emotional, social, and inanimate objects) while scanned in a 7T environment. This allowed us to investigate if the aSTG/STS responded to increasing constituent structure (with increased activity as a function of constituent size) with or without regard to a specific domain of concepts, i.e., social and/or social-emotional content. Activity in the left aSTG/STS was found to increase with constituent size. This region was also modulated by content, however, such that social-emotional concepts were preferred over social and object stimuli. Reading also induced content type effects in domain-specific semantic regions. Those preferring social-emotional content included aSTG/STS, inferior frontal gyrus, posterior STS, lateral fusiform, ventromedial prefrontal cortex, and amygdala, regions included in the "social brain", while those preferring object content included parahippocampal gyrus, retrosplenial cortex, and caudate, regions involved in object processing. These results suggest that semantic content affects higher-level linguistic processing and should be taken into account in future studies.

Trial registration: ClinicalTrials.gov NCT00001360.

Keywords: Affective; Emotion; Language; Social brain; fMRI.

Copyright © 2016. Published by Elsevier Ltd.

Figures

Fig. 1

Example trials and timing for 1-word, 3-word, and 6-word constituent conditions.

Fig. 2

Constituent Size modulated anterior temporal lobe activity. A) Group maps plotted on the TT_N27 anatomy revealed a cluster within left aSTG/STS. B) This cluster demonstrated increasing Constituent Size effects for real words but not jabberwocky. A significant difference between the real word and jabberwocky slopes existed. C) This region also demonstrated a Content Type bias towards Social-Emotional stimuli. The cluster survived multiple comparisons correction (FDR, q = 0.05). The line plot is on a log-linear scale, with best-fit lines fitted to the beta values. Both graphs show percent changes for each condition from the mean signal, which was calculated across all runs, and error bars on graphs indicate ± 1 SEM. Two-sided t-tests were used for all post-hoc tests (***: p < 0.001;**: p < 0.01;*: p < 0.05; t: p < 0.1; n.s.: p > 0.1).

Fig. 3

Domain-specific social/social-emotional and object regions. A) Group average maps plotted on the TT_N27 anatomy reveal left frontal and temporal clusters (L IFG orbitalis, L aSTG, L aSTS, L mSTS, L pSTS, and L lateral fusiform) and plots show these areas most strongly prefer Social-Emotional stimuli followed by Social and Object stimuli. B) Left parahippocampal gyrus (L PHG-1 and PHG-2), L retrosplenial cortex (L RSC), and left caudate clusters display main effects and the accompanying plots show these areas most strongly prefer Object stimuli followed by Social and Social-Emotional stimuli. All clusters survived multiple comparisons correction (FDR, q = 0.05). Graphs show percent changes for each condition from the mean signal, which was calculated across all runs, and error bars on graphs indicate ± 1 SEM. Post-hoc two-sided t-tests were performed between Content Type conditions (***: p < 0.001;**: p < 0.01;*: p < 0.05; t: p < 0.1; n.s.: p > 0.1).