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, Sep 30, 2015
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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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    ABSTRACT: Alexithymia, a deficit in emotional self-awareness, and deficits in empathy, which encompasses the awareness of other's emotions, are related constructs that are both associated with a range of psychopathological disorders. Neuroimaging studies suggest that there is overlap between the neural bases of alexithymia and empathy, but no systematic comparison has been conducted so far. The aim of this structural magnetic resonance imaging study was to disentangle the overlap and differences between the morphological profiles of the cognitive and affective dimensions of alexithymia and empathy, and to find out to what extent these differ between women and men. High-resolution T1 anatomical images were obtained from 125 healthy right-handers (18 - 42 years), 70 women and 55 men. By means of voxel-based morphometry, region of interest (ROI) analyses were performed on gray matter volumes of several anatomically defined a-priori regions previously linked to alexithymia and empathy. Partial correlations were conducted within the female and male group using ROI parameter estimates as dependent variables and the cognitive and affective dimensions of alexithymia and empathy, respectively, as predictors, controlling for age. Results were considered significant if they survived Holm-Bonferroni correction for multiple comparisons. The left amygdala was identified as a key substrate of both alexithymia and empathy. This association was characterized by an opposite pattern: The cognitive alexithymia dimension was linked to smaller, the two empathy dimensions to larger left amygdala volume. While sex-specific effects were not observed for empathy, they were evident for the affective alexithymia dimension: Men - but not women - with difficulty fantasizing had smaller gray matter volume in the middle cingulate cortex. Moreover, structural covariance patterns between the left amygdala and other emotion-related brain regions differed markedly between alexithymia and empathy. These differences may underlie the complex patterns of deficits in emotional self- and other-awareness observed across a range of psychopathological conditions. Copyright © 2015. Published by Elsevier Inc.
    NeuroImage 08/2015; 122. DOI:10.1016/j.neuroimage.2015.08.014 · 6.36 Impact Factor
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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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    ABSTRACT: 'Theory of Mind' refers to the ability to attribute mental states to oneself and other people (Premack & Woodruff, 1978). This study examined the extent to which 'Self' and 'Other' belief-attribution processes within the Theory of Mind (ToM) mechanism could be distinguished behaviourally, and whether these separable components differentially related to Executive Functioning (EF) abilities. A computerized false-belief task, utilizing a matched-design to allow direct comparison of self-oriented vs. other-oriented belief-attribution, was used to assess ToM, and a face-image Stroop task was employed to assess EF, within a population of typically-developed adults. Results revealed significantly longer reaction times when attributing beliefs to other people as opposed to recognizing and attributing beliefs to oneself. Intriguingly, results revealed that 'perspective-shift' requirements (i.e. changing from adoption of the 'self' perspective to the perspective of the 'other', or vice versa) across false-belief trials influenced reaction times. Reaction times were significantly longer when the perspective shift was from self-to-other than from other-to-self. It is suggested that the 'self' forms the stem of understanding the 'other', and is therefore processed regardless of ultimate task demands; in contrast, the 'other' perspective is only processed when explicitly required. We conclude that adopting another person's perspective, even when their belief state is matched to one's own, requires more cognitive effort than recalling and reflecting on self-oriented belief-states. Copyright © 2015 The Authors. Published by Elsevier B.V. All rights reserved.
    Cognition 05/2015; 138. DOI:10.1016/j.cognition.2015.02.001 · 3.63 Impact Factor
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    • "Both the paracentral lobule with its body and spatial representation, and the precuneus, operate together to produce a sense of self, in which the representation of the body and how it acts in space is likely to be an important component (Cavanna and Trimble, 2006). We therefore hypothesize that the reduced functional connectivity of these precuneus/superior parietal cortex (paracentral lobule) regions is related to the altered representation or disconnection of the representation of oneself in the world that may contribute to the reduction in the theory of mind in autism (Lombardo et al., 2010). "
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    ABSTRACT: Whole-brain voxel-based unbiased resting state functional connectivity was analysed in 418 subjects with autism and 509 matched typically developing individuals. We identified a key system in the middle temporal gyrus/superior temporal sulcus region that has reduced cortical functional connectivity (and increased with the medial thalamus), which is implicated in face expression processing involved in social behaviour. This system has reduced functional connectivity with the ventromedial prefrontal cortex, which is implicated in emotion and social communication. The middle temporal gyrus system is also implicated in theory of mind processing. We also identified in autism a second key system in the precuneus/superior parietal lobule region with reduced functional connectivity, which is implicated in spatial functions including of oneself, and of the spatial environment. It is proposed that these two types of functionality, face expression-related, and of one's self and the environment, are important components of the computations involved in theory of mind, whether of oneself or of others, and that reduced connectivity within and between these regions may make a major contribution to the symptoms of autism. © The Author (2015). Published by Oxford University Press on behalf of the Guarantors of Brain.
    Brain 03/2015; 138(5). DOI:10.1093/brain/awv051 · 9.20 Impact Factor
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