Reduced Amygdala-Prefrontal Functional Connectivity in Children With Autism Spectrum Disorder and Co-occurring Disruptive Behavior

Biol Psychiatry Cogn Neurosci Neuroimaging. 2019 Dec;4(12):1031-1041. doi: 10.1016/j.bpsc.2019.01.009. Epub 2019 Feb 4.

Abstract

Background: Disruptive behaviors are prevalent in children with autism spectrum disorder (ASD) and often cause substantial impairments. However, the underlying neural mechanisms of disruptive behaviors remain poorly understood in ASD. In children without ASD, disruptive behavior is associated with amygdala hyperactivity and reduced connectivity with the ventrolateral prefrontal cortex (vlPFC). This study examined amygdala reactivity and connectivity in children with ASD with and without co-occurring disruptive behavior disorders. We also investigated differential contributions of externalizing behaviors and callous-unemotional traits to variance in amygdala connectivity and reactivity.

Methods: This cross-sectional study involved behavioral assessments and neuroimaging in three groups of children 8 to 16 years of age: 18 children had ASD and disruptive behavior, 20 children had ASD without disruptive behavior, and 19 children were typically developing control participants matched for age, gender, and IQ. During functional magnetic resonance imaging, participants completed an emotion perception task of fearful versus calm faces. Task-specific changes in amygdala reactivity and connectivity were examined using whole-brain, psychophysiological interaction, and multiple regression analyses.

Results: Children with ASD and disruptive behavior showed reduced amygdala-vlPFC connectivity compared with children with ASD without disruptive behavior. Externalizing behaviors and callous-unemotional traits were associated with amygdala reactivity to fearful faces in children with ASD after controlling for suppressor effects.

Conclusions: Reduced amygdala-vlPFC connectivity during fear processing may differentiate children with ASD and disruptive behavior from children with ASD without disruptive behavior. The presence of callous-unemotional traits may have implications for identifying differential patterns of amygdala activity associated with increased risk of aggression in ASD. These findings suggest a neural mechanism of emotion dysregulation associated with disruptive behavior in children with ASD.

Keywords: Aggression; Amygdala; Autism; Emotion regulation; Functional connectivity; Ventrolateral prefrontal cortex.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adolescent
  • Amygdala / diagnostic imaging
  • Amygdala / physiopathology*
  • Autism Spectrum Disorder / complications
  • Autism Spectrum Disorder / diagnostic imaging
  • Autism Spectrum Disorder / physiopathology*
  • Behavioral Symptoms / diagnostic imaging
  • Behavioral Symptoms / etiology
  • Behavioral Symptoms / physiopathology*
  • Child
  • Connectome*
  • Cross-Sectional Studies
  • Emotional Regulation / physiology*
  • Facial Expression*
  • Facial Recognition / physiology*
  • Female
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Prefrontal Cortex / diagnostic imaging
  • Prefrontal Cortex / physiopathology*
  • Problem Behavior
  • Social Perception*