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 36:3323–3338, 2015. © 2015 The Authors Human Brain Mapping Published byWiley Periodicals, Inc.
Highlights
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]
A direct correlation has been found between autonomic activity indexed by skin conductance response (SCR) and neural activity in the anterior insular cortex (AIC) measured by functional magnetic resonance imaging during resting state in neurotypical individuals [Eilam-Stock et al, 2014; Fan et al, 2012]
The correlation between d0 and the Empathy Quotient (EQ) was not significant for both groups combined or either group separately (r 5 0.2, P > 0.1). These results are consistent with previous findings on impaired empathy and emotional awareness in ASD individuals [Baron-Cohen and Wheelwright, 2004] and suggest that our visual empathy paradigm was effective in probing the behavioral characteristics related to empathy in ASD
Summary
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]. Previous studies have demonstrated abnormalities in various aspects of empathy in individuals with ASD, including difficulties in mentalizing and perspectivetaking [Fan et al, 2014; Hadjikhani et al, 2014; MinioPaluello et al, 2009], as well as heightened affective arousal to emotional stimuli [Fan et al, 2014; Smith, 2009]. The anterior insular cortex (AIC) and its associated autonomic processing are considered to be crucial in supporting this embodied or interoceptive “theory of mind” [Corradi-Dell’Acqua et al, 2011; Craig, 2014; Gu et al, 2010, 2012; Singer et al, 2009; Wicker et al, 2003]. Accumulating evidence suggests that autonomic signals and their higher-order rerepresentations are crucial for emotional feelings [Craig, 2002; Critchley and Harrison, 2013; Ekman et al, 1983; Gray and Critchley, 2007; Harrison et al, 2010; Rainville et al, 2006]
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