Differential responses of the dorsomedial prefrontal cortex and right posterior superior temporal sulcus to spontaneous mentalizing

Abstract

Previous research suggests a role of the dorsomedial prefrontal cortex (dmPFC) in metacognitive representation of social information, while the right posterior superior temporal sulcus (pSTS) has been linked to social perception. This study targeted these functional roles in the context of spontaneous mentalizing. An animated shapes task was presented to 46 subjects during functional magnetic resonance imaging. Stimuli consisted of video clips depicting animated shapes whose movement patterns prompt spontaneous mentalizing or simple intention attribution. Based on their differential response during spontaneous mentalizing, both regions were characterized with respect to their task-dependent connectivity profiles and their associations with autistic traits. Functional network analyses revealed highly localized coupling of the right pSTS with visual areas in the lateral occipital cortex, while the dmPFC showed extensive coupling with instances of large-scale control networks and temporal areas including the right pSTS. Autistic traits were related to mentalizing-specific activation of the dmPFC and to the strength of connectivity between the dmPFC and posterior temporal regions. These results are in good agreement with the hypothesized roles of the dmPFC and right pSTS for metacognitive representation and perception-based processing of social information, respectively, and further inform their implication in social behavior linked to autism. Hum Brain Mapp 38:3791-3803, 2017. © 2017 Wiley Periodicals, Inc.

Keywords: autistic traits; dorsomedial prefrontal cortex; fMRI; posterior superior temporal sulcus; spontaneous mentalizing.

Figure 1

Animations were presented at the beginning of each trial. Example video clips can be retrieved from https://sites.google.com/site/utafrith/research. Subjects were subsequently asked to categorize the animation to one of the three conditions (R, GD, and ToM), represented by simplified icons. Following ToM videos, subjects were additionally asked to rate the emotional state of each triangle (“How did the small/big triangle feel at the end of the animation?”). Responses were given with the right thumb, using the left, upper, and right key of an MRI compatible button box (Current Designs, PA, USA). As soon as responses were given during MCQ ratings (MCQ‐cat, MCQ‐feeling), the chosen icon was framed in red for the duration of one additional second, followed by a blank screen for the remainder of the respective MCQ phase. No feedback on response accuracy was given. A jitter with variable duration (M = 996 ms, SD = 418 ms) was included before video presentation. [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Whole‐brain connectivity profiles of the (A) dmPFC and (B) right pSTS during spontaneous mentalizing compared to agency perception (PPI_ToM > PPI_GD). For illustrative purposes, a height threshold of t = 3 (P _uncorr = 0.002) was used. Both ROIs, which were used for seed region definition, are illustrated in red. Data are displayed with BrainNet Viewer (http://www.nitrc.org/projects/bnv/). [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Illustration of differences in mentalizing‐specific coupling of the dmPFC (blue) and right pSTS (red) with key regions of the social brain. For each region, the maximum t value (voxel level) is plotted for the mentalizing‐specific contrast (PPI_ToM > PPI_GD), which reflects the difference in connectivity strength during ToM compared to GD animations. The dashed line represents the minimum t value required to pass the significance threshold (P _FWE < 0.05, SVC for the combined mask of social brain regions). TP, temporal pole; aMTG, anterior middle temporal gyrus; pSTS, posterior superior temporal sulcus; dmPFC, dorsomedial prefrontal cortex; IFG, inferior frontal gyrus; L, left; R, right. [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

(A) Sections depicting voxel‐wise associations of mentalizing‐specific activation (i.e., ToM > GD) with autism traits. ROI outlines of dmPFC and right pSTS are overlaid in red. (B) Scatter plot illustrating the association between the individual's total AQ‐K score and contrast estimate of the peak voxel at x = 12, y = 59, z = 28 MNI) within the dmPFC. [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 5

(A) Sections depicting voxel‐wise associations of mentalizing‐specific connectivity of the dmPFC (i.e., PPI_ToM > PPI_GD) with autism traits. ROI outlines of dmPFC and right pSTS are overlaid in red. (B) Scatter plot illustrating the association between total AQ‐K scores and contrast estimates (PPI_ToM > PPI_GD, seed region in the dmPFC) of the peak voxel at x = 57, y = −61, z = 10 (MNI) within the right pSTS ROI. [Color figure can be viewed at http://wileyonlinelibrary.com]