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Cited by 316Autism Spectrum Disorder ResearchNeuroendocrine regulation and behaviorAction Observation and Synchronization

Evaluation of the Social Motivation Hypothesis of Autism: A Systematic Review and Meta-analysis

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Clements, Caitlin C., Zoltowski, Alisa R., Yankowitz, Lisa D., Yerys, Benjamin E., Schultz, Robert T., Herrington, John D.·2018·JAMA Psychiatry
DOI 10.1001/jamapsychiatry.2018.1100PMC PMC6143096
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Abstract

Importance: The social motivation hypothesis posits that individuals with autism spectrum disorder (ASD) find social stimuli less rewarding than do people with neurotypical activity. However, functional magnetic resonance imaging (fMRI) studies of reward processing have yielded mixed results. Objectives: To examine whether individuals with ASD process rewarding stimuli differently than typically developing individuals (controls), whether differences are limited to social rewards, and whether contradictory findings in the literature might be due to sample characteristics. Data Sources: Articles were identified in PubMed, Embase, and PsycINFO from database inception until June 1, 2017. Functional MRI data from these articles were provided by most authors. Study Selection: Publications were included that provided brain activation contrasts between a sample with ASD and controls on a reward task, determined by multiple reviewer consensus. Data Extraction and Synthesis: When fMRI data were not provided by authors, multiple reviewers extracted peak coordinates and effect sizes from articles to recreate statistical maps using seed-based d mapping software. Random-effects meta-analyses of responses to social, nonsocial, and restricted interest stimuli, as well as all of these domains together, were performed. Secondary analyses included meta-analyses of wanting and liking, meta-regression with age, and correlations with ASD severity. All procedures were conducted in accordance with Meta-analysis of Observational Studies in Epidemiology guidelines. Main Outcomes and Measures: Brain activation differences between groups with ASD and typically developing controls while processing rewards. All analyses except the domain-general meta-analysis were planned before data collection. Results: The meta-analysis included 13 studies (30 total fMRI contrasts) from 259 individuals with ASD and 246 controls. Autism spectrum disorder was associated with aberrant processing of both social and nonsocial rewards in striatal regions and increased activation in response to restricted interests (social reward, caudate cluster: d = -0.25 [95% CI, -0.41 to -0.08]; nonsocial reward, caudate and anterior cingulate cluster: d = -0.22 [95% CI, -0.42 to -0.02]; restricted interests, caudate and nucleus accumbens cluster: d = 0.42 [95% CI, 0.07 to 0.78]). Conclusions and Relevance: Individuals with ASD show atypical processing of social and nonsocial rewards. Findings support a broader interpretation of the social motivation hypothesis of ASD whereby general atypical reward processing encompasses social reward, nonsocial reward, and perhaps restricted interests. This meta-analysis also suggests that prior mixed results could be driven by sample age differences, warranting further study of the developmental trajectory for reward processing in ASD.

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  • The first MRI studies of ASD focused on cerebral and cerebellar grey matter and white matter volumes in young children, but were limited by studying toddlers and children aged 18 months or older, missing the opportunity to detect biomarkers of ASD in the first year of life.

    “The first MRI studies of ASD focused on cerebral and cerebellar grey matter and white matter volumes in young children 67,68 , although these studies were limited by studying toddlers and children ≥ 18 months, missing the opportunity to detect biomarkers of ASD in the first year of life.”

    From Autism spectrum disorder (2020) · cites this paper as [67]

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Research works printed but not linked: 2

  1. Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting: Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283 (15):2008-2012.
  2. Constantino JN, Gruber C. The Social Responsiveness Scale. Second Edition (SRS-2).

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Authors
Clements, C. C., Zoltowski, A. R., Yankowitz, L. D., Yerys, B. E., Schultz, R. T., & Herrington, J. D.
Affiliations
Children's Hospital of Philadelphia (US)
Corresponding author
Clements, Caitlin C.
ORCID
Venue
JAMA Psychiatry
Publisher
American Medical Association (AMA)
Published
2018-08-01
Volume
75
Issue
8
Pages
797
ISSN
2168-622X (ISSN-L)
DOI
10.1001/jamapsychiatry.2018.1100
PMC
PMC6143096
OpenAlex
W2808454091
Cited by
316
References
68
Citations by year
2026: 27 · 2025: 41 · 2024: 55 · 2023: 45 · 2022: 35 · 2021: 46 · 2020: 35 · 2019: 27 · 2018: 5
FWCI
3.77
Type
journal article
Language
en
Open access
Locations
  • JAMA Psychiatry (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
National Institute of Mental Health (T32MH064913)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
Keywords
autism spectrum disorder, reward processing, social reward, restricted interests, caudate nucleus, nucleus accumbens, anterior cingulate cortex, ASD severity, neurotypical controls, seed-based d mapping, age effects, sample characteristics
MeSH terms
Autism Spectrum Disorder, Brain, Humans, Magnetic Resonance Imaging, Motivation, Reinforcement, Social, Reward

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