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Atypical neural self-representation in autism

Michael V. Lombardo, Bhismadev Chakrabarti, Edward T. Bullmore, Susan A. Sadek, Greg Pasco, Sally J. Wheelwright, John Suckling, , Simon Baron-Cohen
DOI: http://dx.doi.org/10.1093/brain/awp306 First published online: 14 December 2009

Summary

The ‘self’ is a complex multidimensional construct deeply embedded and in many ways defined by our relations with the social world. Individuals with autism are impaired in both self-referential and other-referential social cognitive processing. Atypical neural representation of the self may be a key to understanding the nature of such impairments. Using functional magnetic resonance imaging we scanned adult males with an autism spectrum condition and age and IQ-matched neurotypical males while they made reflective mentalizing or physical judgements about themselves or the British Queen. Neurotypical individuals preferentially recruit the middle cingulate cortex and ventromedial prefrontal cortex in response to self compared with other-referential processing. In autism, ventromedial prefrontal cortex responded equally to self and other, while middle cingulate cortex responded more to other-mentalizing than self-mentalizing. These atypical responses occur only in areas where self-information is preferentially processed and does not affect areas that preferentially respond to other-referential information. In autism, atypical neural self-representation was also apparent via reduced functional connectivity between ventromedial prefrontal cortex and areas associated with lower level embodied representations, such as ventral premotor and somatosensory cortex. Furthermore, the magnitude of neural self-other distinction in ventromedial prefrontal cortex was strongly related to the magnitude of early childhood social impairments in autism. Individuals whose ventromedial prefrontal cortex made the largest distinction between mentalizing about self and other were least socially impaired in early childhood, while those whose ventromedial prefrontal cortex made little to no distinction between mentalizing about self and other were the most socially impaired in early childhood. These observations reveal that the atypical organization of neural circuitry preferentially coding for self-information is a key mechanism at the heart of both self-referential and social impairments in autism.

  • functional neuroimaging
  • mentalizing
  • self
  • autism
  • Abbreviations:
    Abbreviations
    ADI-R
    Autism Diagnostic Interview Revised
    ADOS
    Autism Diagnostic Observational Schedule
    BA
    Brodmann Area
    BOLD
    blood oxygenated level dependent
    FDR
    false-discovery rate
    fMRI
    functional magnetic resonance imaging
    FO/PMv
    frontal operculum/ventral premotor cortex
    MNI
    Montreal Neurological Institute
    OM
    other-mentalizing
    OP
    other-physical
    PPI
    psychophysiological interaction
    ROI
    region of interest
    SI/SII
    somatosensory cortex
    SM
    self-mentalizing
    SP
    self-physical
    SVC
    small-volume correction
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