Atypical neural self-representation in autism

Autism Research Centre, Douglas House, Cambridge CB2 8AH, UK.
Brain (Impact Factor: 9.2). 12/2009; 133(Pt 2):611-24. DOI: 10.1093/brain/awp306
Source: PubMed


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.

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Available from: Bhismadev Chakrabarti,
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    • "In individuals with ASD, these regions show abnormal gray matter volume (Uddin et al., 2011), abnormal histopathology (Casanova et al., 2006; Oblak et al., 2011), and reduced activation during tasks that require reflecting on emotional states (theory-of-mind and self/other judgments; Castelli et al., 2002; Kana et al., 2014; Lombardo et al., 2010; Uddin et al., 2008). Further, deactivation of DMN regions accurately classified ASD from control subjects (Murdaugh et al., 2012). "
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    • "Regarding the empathy dimensions, lesion studies also suggest a role of the ACC in affective empathy (for a review, see Hillis, 2014). The medial prefrontal cortex (mPFC) and MCC are involved in mentalizing (Lombardo et al., 2010; for a meta-analysis, see Schurz et al., 2014) and the regulation and integration of affect based on their intrinsic connections with the insula (for reviews, see Lamm and Singer, 2010; Medford and Critchley, 2010) and could thus be involved in either empathy dimension. Moreover, its volume seems to be linked to the affective dimension of alexithymia (Goerlich-Dobre et al., 2014a). "
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    • "However, cases in which ToM abilities fail to fully develop or are disrupted due to illness or injury provide evidence for the occurrence of deficits that may differentially affect self and other ToM. For instance, a particular focus of past research has been Autistic Spectrum Conditions (ASC), a defining feature of which is difficulties with ToM abilities (Baron-Cohen, Wheelwright, Hill, Raste, & Plumb, 2001; Brent et al., 2004; Frith, 1989; Hillier & Allinson, 2002; Lombardo et al., 2010). Individuals diagnosed with ASC are often found to display egocentric behaviours in ToM tasks akin to those seen in typically developing children prior to the age of 4-years. "
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