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

https://doi.org/10.1016/j.neubiorev.2015.01.020Get rights and content

Highlights

  • Three major neural systems underlying social information processing are integrated.

  • They are systems for social perception, action observation, and theory of mind.

  • The posterior superior temporal sulcus (pSTS) is uniquely shared across all systems.

  • The pSTS is functionally connected to all other key regions in the three systems.

  • The model has important implications for psychiatric disorders such as autism.

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.

Introduction

The field of social neuroscience is rapidly evolving and with it our understanding of the neural basis of social information processing. Different branches of research within the field have been instrumental in describing specific components of typical and aberrant social information processing. However, these findings are heterogeneous and the field as a whole is lacking a comprehensive model of social information processing. In the following review we outline 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 of social information processing that unites these three central processes and highlight the common brain region implicated in them, the posterior superior temporal sulcus (pSTS) region. We also show that the pSTS region is functionally interconnected to all key regions in the “social brain” for social information processing.

The findings presented in this review are highly relevant for psychiatric research especially regarding a wide variety of seemingly disparate disorders characterized by social deficits (Kennedy and Adolphs, 2012), such as autism spectrum disorder (ASD), Williams syndrome, behavioral-variant frontotemporal dementia, Fragile X, developmental prosopagnosia, Capgras syndrome and psychopathy. To demonstrate how our model can be applied to neuropsychiatric disorders, we use ASD as an example and we review relevant evidence suggesting that one or more of the key regions in our model are abnormal in ASD. As defined in DSM-5, ASD is a disorder characterized by persistent and prominent deficits in social communication and social interaction as well as restricted and repetitive behavior (APA, 2013). We also discuss the implications of our model for research on ASD, highlighting the temporal integration role of the pSTS and a recent hypothesis that posits that ASD can be understood as a disorder of temporal prediction (Sinha et al., 2014). Our model also suggests that the pSTS region may serve as a target for interventions designed to improve social functioning in ASD (e.g., Ventola et al., 2014).

Section snippets

A neural system for social perception

Humans are inherently social creatures as evidenced by a range of social behavior that typically emerges early in infancy. Infants preferentially orient to social signals such as facial expressions and by the age of three months recognize their mother's face and tone of voice (Johnson et al., 1991, Kovacs et al., 2010, Kurzweil, 1988, Valenza et al., 1996). Expertise in social perception, defined as the ability to decode another person's mental states based on basic behavioral signals, is

A neural system for action observation

While social perception involves perceiving and decoding others’ external behavioral signals and inferring their underlying intentions, the role of the perceiver's self is relatively silent. However, when people understand others’ actions, there is another mechanism that relies heavily on the perceiver's self: the perceiver may try to understand what the actions would mean if they themselves were to perform the same actions. In this route, the role of the perceiver's self is much more prominent

A neural system for theory of mind

Over the past two decades, research on theory of mind (also referred to as mentalizing or mental state reasoning) has provided important insights into social function and dysfunction. Theory of mind has been defined as the ability to predict the relationships between external states of affairs and internal states of mind (Frith, 1989). This ability requires decoupling one's subjective reality from the reality that others perceive (Baillargeon et al., 2010, Blakemore et al., 2007, Frith and

An integrative model of social information processing

Upon reviewing the three major neural systems underlying social information processing, a picture emerges of the pSTS at the intersection of social perception, action observation, and theory of mind. The pSTS supports social information processing on multiple levels. It is involved in the temporal integration of visual, auditory and somatosensory cues of others’ behaviors and representation of a basic form of intentionality (Beauchamp et al., 2008, Gordon et al., 2013, Hagan et al., 2009, Hagan

Conclusion

In this paper, we reviewed and integrated three major neural systems underlying social information processing: social perception, action observation, and theory of mind, which have almost exclusively been studied in isolation. Comparing and synthesizing these three key systems, our integrative neural model not only summarizes the regions implicated in each neural system but also provides an overall map advancing the relationships among them. We also reviewed evidence of aberrant social

Acknowledgements

This work was supported by Hilibrand Autism Fellowships from the Yale Child Study Center to D. Yang and G. Rosenblau and by an Autism Speaks Meixner Postdoctoral Fellowship in Translational Research (#9284) to D. Yang.

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