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.

Oxytocin selectively modulates brain response to stimuli probing social synchrony

“…In response to CS, OT attenuated (in pSTS) or reversed (in IFG) group differences, whereas in response to SS, OT induced activity (in IPL) in combat-trained veterans. Given the integrative role of the pSTS in social perception, action observation, and theory-of-mind (Yang et al, 2015), the increased recruitment of this area by combattrained participants likely reflects stress-related over-activity, possibly related to increased sensory re-experiencing of combat-related cues. Such over-activity of the pSTS under PBO was attenuated under OT, thereby possibly reflecting an anxiolytic influence of OT on stress-induced brain activation.…”

“…Generally, the pSTS has not been proposed as exclusively supporting mirror system functioning; rather, it has also been implicated in mentalizing and social perception (Dufour et al, 2013). Researchers have pointed to the integrative role of pSTS in all three systems and have demonstrated its connection to other regions in each system (Yang et al, 2015). Hence, in contrast to the IPL and IFG that exclusively underpin mirroring in social contexts, the pSTS additionally extracts social and intentional cues to facilitate mental inference.…”

Distinct neural bases of disruptive behavior and autism symptom severity in boys with autism spectrum disorder

“…For example, neuroimaging studies consistently show that the posterior superior temporal sulcus (pSTS), fusiform gyrus (FFG), and inferior frontal gyrus (IFG) are key regions for social information processing [2] and individuals with ASD relative to typically developing (TD) controls exhibited hypoactivation in these regions [3, 4]. However, ASD often co-occurs with other psychiatric disorders [5, 6], such as anxiety disorder [7], attention-deficit/hyperactivity disorder (ADHD) [8], and oppositional defiant disorder (ODD) [9].…”

“…The two contrasts in the biological motion task, namely, social perception (BIO > SCR) and DMN deactivation (fixation > BIO), afford the opportunity to compare these two neural bases within the same sample of children with ASD. We hypothesize that there would be distinct and separable neural bases of disruptive behavior and autism symptom severity in ASD, in which (a) autism symptom severity would be associated with less activation in the social perception circuitry [2] and (b) disruptive behavior would be associated with less DMN deactivation. We also explored co-occurring anxiety and ADHD symptoms [6] as potential mediators of the neural basis of disruptive behavior.…”

What can autism teach us about the role of sensorimotor systems in higher cognition? New clues from studies on language, action semantics, and abstract emotional concept processing

“…Functional (Yang, Rosenblau, Keifer, & Pelphrey, 2015) and anatomical (Herbet et al, 2014) data suggest there are multiple routes to understanding other minds and multiple systems which typically interact in doing so e an interaction which is conspicuously atypical in autism (Fishman, Keown, Lincoln, Pineda, & Mü ller, 2014). These interacting systems include 'higher-order' mentalizing areas (ventromedial prefrontal cortex, cingulate cortex and temporoparietal junction) and 'lower-order' simulatory areas (premotor and somatosensory cortex, the frontoparietal mirror network) (Centelles, Assaiante, Nazarian, Anton, & Schmitz, 2011;Herbet et al, 2014;Keysers & Gazzola, 2007;Schippers, Roebroeck, Renken, Nanetti, & Keysers, 2010;Sperduti, Guionnet, Fossati, & Nadel, 2014;Spunt & Lieberman, 2012;Zaki, Weber, Bolger, & Ochsner, 2009).…”