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Published April 8, 2015 | Published
Journal Article Open

Idiosyncratic Brain Activation Patterns Are Associated with Poor Social Comprehension in Autism

Abstract

Autism spectrum disorder (ASD) features profound social deficits but neuroimaging studies have failed to find any consistent neural signature. Here we connect these two facts by showing that idiosyncratic patterns of brain activation are associated with social comprehension deficits. Human participants with ASD (N = 17) and controls (N = 20) freely watched a television situation comedy (sitcom) depicting seminaturalistic social interactions ("The Office", NBC Universal) in the scanner. Intersubject correlations in the pattern of evoked brain activation were reduced in the ASD group—but this effect was driven entirely by five ASD subjects whose idiosyncratic responses were also internally unreliable. The idiosyncrasy of these five ASD subjects was not explained by detailed neuropsychological profile, eye movements, or data quality; however, they were specifically impaired in understanding the social motivations of characters in the sitcom. Brain activation patterns in the remaining ASD subjects were indistinguishable from those of control subjects using multiple multivariate approaches. Our findings link neurofunctional abnormalities evoked by seminaturalistic stimuli with a specific impairment in social comprehension, and highlight the need to conceive of ASD as a heterogeneous classification.

Additional Information

© 2015 the authors. Beginning six months after publication the Work will be made freely available to the public on SfN's website to copy, distribute, or display under a Creative Commons Attribution 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/). Received Dec. 15, 2014; revised Feb. 25, 2015; accepted March 1, 2015. This work was supported by the National Institutes of Health Grant K99MH094409 / R00MH094409 (D.P.K.), NARSAD Young Investigator Award from the Brain and Behavior Research Foundation (D.P.K.), Simons Foundation SFARI-07-01 (R.A.), National Institutes of Mental Health Conte Center P50MH094258 (R.A.), and a National Science Foundation Graduate Research Fellowship (L.B.). We thank Lynn K. Paul for assistance with clinical diagnoses, Catherine Holcomb and Tim Armstrong for assistance with scheduling and testing of participants, and Haley Gedek and Susannah Burkholder for assistance in scoring the comprehension task. Author contributions: J.M.T., R.A., and D.P.K. designed research; D.P.K. performed research; L.B., J.D., J.M.T., and D.P.K. analyzed data; L.B., J.D., R.A., and D.P.K. wrote the paper.

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Created:
August 22, 2023
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October 23, 2023