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Original Investigation |

Evaluation of Quantified Social Perception Circuit Activity as a Neurobiological Marker of Autism Spectrum Disorder

Malin Björnsdotter, MSc, PhD1,2; Nancy Wang3; Kevin Pelphrey4; Martha D. Kaiser3
[+] Author Affiliations
1Center for Social and Affective Neuroscience, Department of Clinical and Experimental Medicine, Linköping University, Linköping, Sweden
2Institute of Neuroscience and Physiology, University of Gothenburg, Gothenburg, Sweden
3Center for Translational Developmental Neuroscience, Child Study Center, Yale School of Medicine, New Haven, Connecticut
4Autism And Neurodevelopment Disorders Institute, The George Washington University and Children's National Medical Center, Washington, DC
JAMA Psychiatry. 2016;73(6):614-621. doi:10.1001/jamapsychiatry.2016.0219.
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Importance  Autism spectrum disorder (ASD) is marked by social disability and is associated with dysfunction in brain circuits supporting social cue perception. The degree to which neural functioning reflects individual-level behavioral phenotype is unclear, slowing the search for functional neuroimaging biomarkers of ASD.

Objective  To examine whether quantified neural function in social perception circuits may serve as an individual-level marker of ASD in children and adolescents.

Design, Setting, and Participants  The cohort study was conducted at the Yale Child Study Center and involved children and adolescents diagnosed as having ASD and typically developing participants. Participants included a discovery cohort and a larger replication cohort. Individual-level social perception circuit functioning was assessed as functional magnetic resonance imaging brain responses to point-light displays of coherent vs scrambled human motion.

Main Outcomes and Measures  Outcome measures included performance of quantified brain responses in affected male and female participants in terms of area under the receiver operating characteristic curve (AUC), sensitivity and specificity, and correlations between brain responses and social behavior.

Results  Of the 39 participants in the discovery cohort aged 4 to 17 years, 22 had ASD and 30 were boys. Of the 75 participants in the replication cohort aged 7 to 20 years, 37 had ASD and 52 were boys. A relative reduction in social perception circuit responses was identified in discovery cohort boys with ASD at an AUC of 0.75 (95% CI, 0.52-0.89; P = .01); however, typically developing girls and girls with ASD could not be distinguished (P = .54). The results were confirmed in the replication cohort, where brain responses were identified in boys with ASD at an AUC of 0.79 (95% CI, 0.64-0.91; P < .001) and failed to distinguish affected and unaffected girls (P = .82). Across both cohorts, boys were identified at an AUC of 0.77 (95% CI, 0.64-0.86) with corresponding sensitivity and specificity of 76% each. Additionally, brain responses were associated with social behavior in boys but not in girls.

Conclusions and Relevance  Quantified social perception circuit activity is a promising individual-level candidate neural marker of the male ASD behavioral phenotype. Our findings highlight the need to better understand effects of sex on social perception processing in relation to ASD phenotype manifestations.

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Figure.
Performance of Quantified Social Perception Circuit Activity in Detecting Autism Spectrum Disorder

A, The social perception circuit defined in the replication cohort, autism spectrum disorder and typically developing combined, from the group-level main effect for the contrast (coherent>scrambled motion) (P < .0001, k > 6). Receiver operating characteristic curves for detecting children diagnosed as having autism spectrum disorder based on social perception circuit response levels for girls (B), all boys (C), and boys matched on cognitive ability (D). The association between social perception circuit response levels (average β values) and social behavior (Social Responsiveness Scale scores) for girls (E) and boys (F). The open squares and circles indicate typically developing responses, and the closed squares and circles indicate autism spectrum disorder responses. The r and P values indicate tests for negative partial correlations, corrected for age. AUC indicates area under the receiver operating characteristic curve.

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