Common and distinct networks for self-referential and social stimulus processing in the human brain

Self-referential processing is a complex cognitive function, involving a set of implicit and explicit processes, complicating investigation of its distinct neural signature. The present study explores the functional overlap and dissociability of self-referential and social stimulus processing. We combined an established paradigm for explicit self-referential processing with an implicit social stimulus processing paradigm in one fMRI experiment to determine the neural effects of self-relatedness and social processing within one study. Overlapping activations were found in the orbitofrontal cortex and in the intermediate part of the precuneus. Stimuli judged as self-referential specifically activated the posterior cingulate cortex, the ventral medial prefrontal cortex, extending into anterior cingulate cortex and orbitofrontal cortex, the dorsal medial prefrontal cortex, the ventral and dorsal lateral prefrontal cortex, the left inferior temporal gyrus, and occipital cortex. Social processing specifically involved the posterior precuneus and bilateral temporo-parietal junction. Taken together, our data show, not only, first, common networks for both processes in the medial prefrontal and the medial parietal cortex, but also, second, functional differentiations for self-referential processing versus social processing: an anterior–posterior gradient for social processing and self-referential processing within the medial parietal cortex and specific activations for self-referential processing in the medial and lateral prefrontal cortex and for social processing in the temporo-parietal junction.

[1]  R. Saxe,et al.  Making sense of another mind: The role of the right temporo-parietal junction , 2005, Neuropsychologia.

[2]  A. Goldman,et al.  Mirror neurons and the simulation theory of mind-reading , 1998, Trends in Cognitive Sciences.

[3]  Kevin N. Ochsner,et al.  The neural correlates of direct and reflected self-knowledge , 2005, NeuroImage.

[4]  F. Heider,et al.  An experimental study of apparent behavior , 1944 .

[5]  Daniel P. Kennedy,et al.  The social brain in psychiatric and neurological disorders , 2012, Trends in Cognitive Sciences.

[6]  C. Keysers,et al.  Integrating simulation and theory of mind: from self to social cognition , 2007, Trends in Cognitive Sciences.

[7]  M. First,et al.  Structured clinical interview for DSM-IV axis I disorders : SCID-I: clinical version : administration booklet , 1996 .

[8]  Kevin N. Ochsner,et al.  A Meta-analysis of Functional Neuroimaging Studies of Self- and Other Judgments Reveals a Spatial Gradient for Mentalizing in Medial Prefrontal Cortex , 2012, Journal of Cognitive Neuroscience.

[9]  Daniel S. Margulies,et al.  Delineating self-referential processing from episodic memory retrieval: Common and dissociable networks , 2010, NeuroImage.

[10]  Marc Jeannerod,et al.  Modulating the experience of agency: a positron emission tomography study , 2003, NeuroImage.

[11]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[12]  A. Bailey,et al.  Are there theory of mind regions in the brain? A review of the neuroimaging literature , 2009, Human brain mapping.

[13]  Rebecca Saxe,et al.  Overlapping and non-overlapping brain regions for theory of mind and self reflection in individual subjects. , 2006, Social cognitive and affective neuroscience.

[14]  M. Erb,et al.  Observing one’s hand become anarchic: An fMRI study of action identification , 2003, Consciousness and Cognition.

[15]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[16]  Rajesh P. N. Rao,et al.  "Social" robots are psychological agents for infants: A test of gaze following , 2010, Neural Networks.

[17]  H. Sackeim,et al.  Parietal cortex and representation of the mental Self. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[18]  K. Blair,et al.  The influence of valence and decision difficulty on self-referential processing , 2013, Front. Hum. Neurosci..

[19]  Hongkeun Kim,et al.  A dual-subsystem model of the brain's default network: Self-referential processing, memory retrieval processes, and autobiographical memory retrieval , 2012, NeuroImage.

[20]  P. Lang International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[21]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[22]  C. Frith,et al.  Experiencing Oneself vs Another Person as Being the Cause of an Action: The Neural Correlates of the Experience of Agency , 2002, NeuroImage.

[23]  Jennifer A. Mangels,et al.  Predictive Codes for Forthcoming Perception in the Frontal Cortex , 2006, Science.

[24]  Jason P. Mitchell,et al.  Medial prefrontal dissociations during processing of trait diagnostic and nondiagnostic person information. , 2006, Social cognitive and affective neuroscience.

[25]  John Suckling,et al.  Shared Neural Circuits for Mentalizing about the Self and Others , 2010, Journal of Cognitive Neuroscience.

[26]  K. Ochsner,et al.  The role of social cognition in emotion , 2008, Trends in Cognitive Sciences.

[27]  Julian M. Pine,et al.  Constructing a Language: A Usage-Based Theory of Language Acquisition. , 2004 .

[28]  F. Overwalle Social cognition and the brain: a meta-analysis. , 2009 .

[29]  J. Stevenson The cultural origins of human cognition , 2001 .

[30]  Chad E. Forbes,et al.  The role of the human prefrontal cortex in social cognition and moral judgment. , 2010, Annual review of neuroscience.

[31]  Justin L. Vincent,et al.  Precuneus shares intrinsic functional architecture in humans and monkeys , 2009, Proceedings of the National Academy of Sciences.

[32]  G. Gallup,et al.  Where am I? The neurological correlates of self and other. , 2004, Brain research. Cognitive brain research.

[33]  S. Gallagher Philosophical conceptions of the self: implications for cognitive science , 2000, Trends in Cognitive Sciences.

[34]  J. Müller,et al.  Of the brain. , 1837 .

[35]  Georg Northoff,et al.  Self-referential processing in our brain—A meta-analysis of imaging studies on the self , 2006, NeuroImage.

[36]  G. Humphreys,et al.  Self-referential processing is distinct from semantic elaboration: Evidence from long-term memory effects in a patient with amnesia and semantic impairments , 2013, Neuropsychologia.

[37]  M. First,et al.  Structured clinical interview for DSM-IV axis II personality disorders : SCID-II , 1997 .

[38]  P. Ruby,et al.  What is self-specific? Theoretical investigation and critical review of neuroimaging results. , 2009, Psychological review.

[39]  M. Tomasello The Cultural Origins of Human Cognition , 2000 .

[40]  C. Frith,et al.  Movement and Mind: A Functional Imaging Study of Perception and Interpretation of Complex Intentional Movement Patterns , 2000, NeuroImage.

[41]  G. Fink,et al.  Minds at rest? Social cognition as the default mode of cognizing and its putative relationship to the “default system” of the brain , 2008, Consciousness and Cognition.

[42]  Michael J. Brammer,et al.  The role of ‘shared representations’ in social perception and empathy: An fMRI study , 2006, NeuroImage.

[43]  Jennifer S. Beer,et al.  Social cognition: A multi level analysis , 2006, Brain Research.

[44]  Matthew D. Lieberman,et al.  Integrating automatic and controlled processes into neurocognitive models of social cognition , 2006, Brain Research.

[45]  Hans-Jochen Heinze,et al.  Differential parametric modulation of self‐relatedness and emotions in different brain regions , 2009, Human brain mapping.

[46]  F. Bermpohl,et al.  Cortical midline structures and the self , 2004, Trends in Cognitive Sciences.

[47]  P. Downing,et al.  The neural basis of visual body perception , 2007, Nature Reviews Neuroscience.

[48]  K. Vogeley,et al.  Toward a second-person neuroscience 1 , 2013, Behavioral and Brain Sciences.