The effects of intranasal oxytocin on reward circuitry responses in children with autism spectrum disorder

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  • Greene, R. K
    • Affiliation: College of Arts and Sciences, Department of Psychology and Neuroscience
  • Spanos, M.
    • Affiliation: School of Medicine, Neurodevelopment Disorders Research Center, Carolina Institute for Developmental Disabilities
    • Other Affiliation: Duke Clinical Research Institute, Duke University, Durham, USA; Duke Center for Autism and Brain Development, Duke University, Durham, USA; Department of Psychiatry and Behavioral Sciences, Duke University Medical Center, Durham, USA
  • Alderman, Cheryl
    • Affiliation: School of Medicine, Neurodevelopment Disorders Research Center, Carolina Institute for Developmental Disabilities
    • Other Affiliation: Duke Clinical Research Institute, Duke University, Durham, USA
  • Walsh, Erin C
    • Affiliation: School of Medicine, Department of Psychiatry
  • Bizzell, J.
    • Other Affiliation: Duke-UNC Brain Imaging and Analysis Center, Duke University Medical Center, Durham, USA
  • Mosner, Maya G
    • Affiliation: School of Medicine, Neurodevelopment Disorders Research Center, Carolina Institute for Developmental Disabilities
  • Kinard, Jessica
    • Affiliation: School of Medicine, Neurodevelopment Disorders Research Center, Carolina Institute for Developmental Disabilities
  • Stuber, G. D
    • Affiliation: School of Medicine, Department of Cell Biology and Physiology
  • Chandrasekhar, T.
    • Affiliation: School of Medicine, Department of Psychiatry
    • Other Affiliation: Duke Center for Autism and Brain Development, Duke University, Durham, USA
  • Politte, L. C
    • Affiliation: School of Medicine, Neurodevelopment Disorders Research Center, Carolina Institute for Developmental Disabilities
  • Sikich, Linmarie
    • Affiliation: School of Medicine, Department of Psychiatry
    • Other Affiliation: Duke Clinical Research Institute, Duke University, Durham, USA; Duke Center for Autism and Brain Development, Duke University, Durham, USA; Department of Psychiatry and Behavioral Sciences, Duke University Medical Center, Durham, USA
  • Dichter, Gabriel
    • Affiliation: College of Arts and Sciences, Department of Psychology and Neuroscience
Abstract
  • Background Intranasal oxytocin (OT) has been shown to improve social communication functioning of individuals with autism spectrum disorder (ASD) and, thus, has received considerable interest as a potential ASD therapeutic agent. Although preclinical research indicates that OT modulates the functional output of the mesocorticolimbic dopamine system that processes rewards, no clinical brain imaging study to date has examined the effects of OT on this system using a reward processing paradigm. To address this, we used an incentive delay task to examine the effects of a single dose of intranasal OT, versus placebo (PLC), on neural responses to social and nonsocial rewards in children with ASD. Methods In this placebo-controlled double-blind study, 28 children and adolescents with ASD (age: M = 13.43 years, SD = 2.36) completed two fMRI scans, one after intranasal OT administration and one after PLC administration. During both scanning sessions, participants completed social and nonsocial incentive delay tasks. Task-based neural activation and connectivity were examined to assess the impact of OT relative to PLC on mesocorticolimbic brain responses to social and nonsocial reward anticipation and outcomes. Results Central analyses compared the OT and PLC conditions. During nonsocial reward anticipation, there was greater activation in the right nucleus accumbens (NAcc), left anterior cingulate cortex (ACC), bilateral orbital frontal cortex (OFC), left superior frontal cortex, and right frontal pole (FP) during the OT condition relative to PLC. Alternatively, during social reward anticipation and outcomes, there were no significant increases in brain activation during the OT condition relative to PLC. A Treatment Group × Reward Condition interaction revealed relatively greater activation in the right NAcc, right caudate nucleus, left ACC, and right OFC during nonsocial relative to social reward anticipation during the OT condition relative to PLC. Additionally, these analyses revealed greater activation during nonsocial reward outcomes during the OT condition relative to PLC in the right OFC and left FP. Finally, functional connectivity analyses generally revealed changes in frontostriatal connections during the OT condition relative to PLC in response to nonsocial, but not social, rewards. Conclusions The effects of intranasal OT administration on mesocorticolimbic brain systems that process rewards in ASD were observable primarily during the processing of nonsocial incentive salience stimuli. These findings have implications for understanding the effects of OT on neural systems that process rewards, as well as for experimental trials of novel ASD treatments developed to ameliorate social communication impairments in ASD.
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  • Article
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  • In Copyright
Rights holder
  • The Author(s).
Journal title
  • Journal of Neurodevelopmental Disorders
Journal volume
  • 10
Journal issue
  • 1
Page start
  • 12
Language
  • English
Bibliographic citation
  • Journal of Neurodevelopmental Disorders. 2018 Mar 27;10(1):12
Publisher
  • BioMed Central

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