Self Responses along Cingulate Cortex Reveal Quantitative Neural Phenotype for High-Functioning Autism

Computational Psychiatry Unit, Baylor College of Medicine, Houston, TX 77030, USA.
Neuron (Impact Factor: 15.05). 03/2008; 57(3):463-73. DOI: 10.1016/j.neuron.2007.12.020
Source: PubMed


Attributing behavioral outcomes correctly to oneself or to other agents is essential for all productive social exchange. We approach this issue in high-functioning males with autism spectrum disorder (ASD) using two separate fMRI paradigms. First, using a visual imagery task, we extract a basis set for responses along the cingulate cortex of control subjects that reveals an agent-specific eigenvector (self eigenmode) associated with imagining oneself executing a specific motor act. Second, we show that the same self eigenmode arises during one's own decision (the self phase) in an interpersonal exchange game (iterated trust game). Third, using this exchange game, we show that ASD males exhibit a severely diminished cingulate self response when playing the game with a human partner. This diminishment covaries parametrically with their behaviorally assessed symptom severity, suggesting its value as an objective endophenotype. These findings may provide a quantitative assessment tool for high-functioning ASD.

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Available from: Kenneth Kishida, Mar 12, 2014
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    • "Autism spectrum disorder (ASD) is a family of neurodevelopmental disorders with a wide range of sensory and socio-emotional deficits [Chiu et al., 2008; Dinstein et al., 2012; Happe et al., 2006]. Empathy, the ability to share vicariously the feelings of others, is an important socialemotional faculty [Gu et al., 2010; Moriguchi et al., 2007] and is compromised in individuals with ASD [Baron- Cohen and Wheelwright, 2004]. "
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    ABSTRACT: Accumulating evidence suggests that autonomic signals and their cortical representations are closely linked to emotional processes, and that related abnormalities could lead to social deficits. Although socio-emotional impairments are a defining feature of autism spectrum disorder (ASD), empirical evidence directly supporting the link between autonomic, cortical, and socio-emotional abnormalities in ASD is still lacking. In this study, we examined autonomic arousal indexed by skin conductance responses (SCR), concurrent cortical responses measured by functional magnetic resonance imaging, and effective brain connectivity estimated by dynamic causal modeling in seventeen unmedicated high-functioning adults with ASD and seventeen matched controls while they performed an empathy-for-pain task. Compared to controls, adults with ASD showed enhanced SCR related to empathetic pain, along with increased neural activity in the anterior insular cortex, although their behavioral empathetic pain discriminability was reduced and overall SCR was decreased. ASD individuals also showed enhanced correlation between SCR and neural activities in the anterior insular cortex. Importantly, significant group differences in effective brain connectivity were limited to greater reduction in the negative intrinsic connectivity of the anterior insular cortex in the ASD group, indicating a failure in attenuating anterior insular responses to empathetic pain. These results suggest that aberrant interoceptive precision, as indexed by abnormalities in autonomic activity and its central representations, may underlie empathy deficits in ASD. Hum Brain Mapp, 2015. © 2015 Wiley Periodicals, Inc. © 2015 Wiley Periodicals, Inc.
    Full-text · Article · May 2015 · Human Brain Mapping
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    • "The final complexity arises when we consider that although it is common in experimental economics to create one-shot interactions, many of the most interesting and richest aspects of behaviour arise with multiple rounds of interactions. Here, for concreteness, we consider the multi round trust task, which is a social exchange game that has been used with hundreds of pairs (dyads) of subjects, including both normal and clinical populations [14] [15] [16] [17] [18]. This game has been used to show that characteristics that only arise in multi-round interactions such as defection (agent A increases their cooperation between two rounds; agent B responds by decreasing theirs) have observable neural consequences that can be measured using functional magnetic resonance imaging (fMRI) [19] [14] [20] [21] [22]. "
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    ABSTRACT: Reciprocating interactions represent a central feature of all human exchanges. They have been the target of various recent experiments, with healthy participants and psychiatric populations engaging as dyads in multi-round exchanges such as a repeated trust task. Behaviour in such exchanges involves complexities related to each agent's preference for equity with their partner, beliefs about the partner's appetite for equity, beliefs about the partner's model of their partner, and so on. Agents may also plan different numbers of steps into the future. Providing a computationally precise account of the behaviour is an essential step towards understanding what underlies choices. A natural framework for this is that of an interactive partially observable Markov decision process (IPOMDP). However, the various complexities make IPOMDPs inordinately computationally challenging. Here, we show how to approximate the solution for the multi-round trust task using a variant of the Monte-Carlo tree search algorithm. We demonstrate that the algorithm is efficient and effective, and therefore can be used to invert observations of behavioural choices. We use generated behaviour to elucidate the richness and sophistication of interactive inference.
    Full-text · Article · Feb 2015 · PLoS Computational Biology
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    • "This result is consistent with the findings of previous studies that suggest a link between fairnessrelated behavior and theory of mind, providing further support to this claim from a new angle (Chiu et al., 2008; Frith & Frith, 2008; Jensen, Call, & Tomasselo, 2007; McCabe, Houser, Ryan, Smith, & Trouard, 2001; Sally & Hill, 2006). For instance, studies using functional magnetic resonance imaging (fMRI) found that brain areas related to theory of mind (medial prefrontal cortex) were activated as adult participants behaved cooperatively in a trust game (McCabe et al., 2001), whereas another recent study found that, compared with control adult participants, adult men with ASD showed reduced activity in the mid-cingulate cortex, an area thought to be related to cognitions of the self acting in a social context, when deciding to trust one's partner in a trust game (Chiu et al., 2008). This result is speculated to arise from the lack of ability of autistic adults to simulate their reputation in the eyes of others (Frith & Frith, 2008). "

    Full-text · Dataset · Oct 2014
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