Autonomic and brain responses associated with empathy deficits in autism spectrum disorder

Hum Brain Mapp. 2015 Sep;36(9):3323-38. doi: 10.1002/hbm.22840. Epub 2015 May 21.

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.

Keywords: autism spectrum disorder; autonomic nervous system; brain connectivity; dynamic causal modeling; empathy; functional magnetic resonance imaging; interoceptive inference.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Autism Spectrum Disorder / physiopathology*
  • Autism Spectrum Disorder / psychology*
  • Bayes Theorem
  • Brain / physiopathology*
  • Brain Mapping / methods
  • Discrimination, Psychological
  • Empathy / physiology*
  • Galvanic Skin Response / physiology*
  • Humans
  • Linear Models
  • Magnetic Resonance Imaging / methods
  • Male
  • Models, Neurological
  • Neural Pathways / physiopathology
  • Neuropsychological Tests
  • Pain / psychology
  • Signal Processing, Computer-Assisted