An integrative neural model of social perception, action observation, and theory of mind

Abstract

In the field of social neuroscience, major branches of research have been instrumental in describing independent components of typical and aberrant social information processing, but the field as a whole lacks a comprehensive model that integrates different branches. We review existing research related to the neural basis of three key neural systems underlying social information processing: social perception, action observation, and theory of mind. We propose an integrative model that unites these three processes and highlights the posterior superior temporal sulcus (pSTS), which plays a central role in all three systems. Furthermore, we integrate these neural systems with the dual system account of implicit and explicit social information processing. Large-scale meta-analyses based on Neurosynth confirmed that the pSTS is at the intersection of the three neural systems. Resting-state functional connectivity analysis with 1000 subjects confirmed that the pSTS is connected to all other regions in these systems. The findings presented in this review are specifically relevant for psychiatric research especially disorders characterized by social deficits such as autism spectrum disorder.

Keywords: Action observation; Autism spectrum disorder; Functional connectivity; Imitation; Mentalizing; Mirror system; Neural systems; Posterior superior temporal sulcus; Psychiatric disorders; Social information processing; Social neuroscience; Social perception; Theory of mind.

Fig. 1

An integrative model of the neural systems for social information processing: social perception, action observation, and theory of mind. Dashed lines suggest possible connections among these systems. AMY, amygdala; FFG, fusiform gyrus; OFC, orbitofrontal cortex; pSTS, posterior superior temporal sulcus; IFG, inferior frontal gyrus; IPL, inferior parietal lobule; MPFC, medial prefrontal cortex; TPJ, temporo-parietal junction; PCC/PC, posterior cingulate cortex/precuneus; ATL, anterior temporal lobe.

Fig. 2

Brain regions engaged during: (A) social perception, (B) action observation, and (C) theory of mind/mentalizing, as reported by the large-scale, meta-analytical tool Neurosynth (reverse inference, FDR q<.01). Figure (D) is the conjunction of (A)-(C). The only common region was localized to the right pSTS, center of gravity=(52, −46, 9), MNI152 mm coordinate. Figure (E) is the word cloud of the top 30 psychological terms most strongly associated with the right pSTS region as shown in Figure (D); the terms were generated via the decode function of Neurosynth.

Fig. 3

Resting-state functional connectivity with a sample of 1000 subjects and a seed voxel in the pSTS at (52, −46, 9), MNI152mm coordinate, i.e., the center of gravity in Fig. 2(D). The result was the average of the results based on seed voxels at (52, −46, 10) and (52, −46, 8) and the maps were available from the Neurosynth website. The strength of functional connectivity is based on correlations, with higher values indicating greater similarity in activation between the seed voxel in the pSTS and other voxels of the brain. For details of these maps, see Yeo et al. (2011), Buckner et al. (2011), and Choi et al. (2012). Top Panel (A) shows that the pSTS is functionally connected to the major regions implicated in social information processing (see the integrated model in Fig. 1). Bottom Panel (B) shows functional connectivity from the seed voxel in the pSTS to cerebellar cortex. The slice was at (-19, −76, −41), MNI152mm coordinate.