Neural modulation of social reinforcement learning by intranasal oxytocin in male adults with high-functioning autism spectrum disorder: a randomized trial
Open accessAbstract
Reduced social motivation is a hallmark of individuals with autism spectrum disorders (ASDs). Although the exact neural mechanisms are unclear, oxytocin has been shown to enhance motivation and attention to social stimuli, suggesting a potential to augment social reinforcement learning as the central mechanism of behavioral interventions in ASD. We tested how reinforcement learning in social contexts and associated reward prediction error (RPE) signals in the nucleus accumbens (NAcc) were modulated by intranasal oxytocin. Male adults with a childhood diagnosis of ASD (n = 15) and healthy controls (n = 24; aged 18-26 years) performed a probabilistic reinforcement learning task during functional magnetic resonance imaging in a single-center (research center in Germany), randomized double-blind, placebo-controlled cross-over trial. The interventions were intranasal oxytocin (Syntocinon®, Novartis; 10 puffs = 20 international units (IUs) per treatment) and placebo spray. Using computational modeling of behavioral data, trial-by-trial RPE signals were assessed and related to brain activation in NAcc during reinforcing feedback in social and non-social contexts. The order of oxytocin/placebo was randomized for 60 participants. Twenty-one participants were excluded from analyses, leaving 39 for the final analysis. Behaviorally, individuals with ASD showed enhanced learning under oxytocin when the learning target as well as feedback was social as compared to non-social (social vs. non-social target: 87.09% vs. 71.29%, 95% confidence interval (CI): 7.28-24.33, p = .003; social vs. non-social feedback: 81.00% vs. 71.29%, 95% CI: 2.81-16.61, p = .027). Correspondingly, oxytocin enhanced the correlation of the RPE signal with NAcc activation during social (vs. non-social) feedback in ASD (3.48 vs. -1.12, respectively, 95% CI: 2.98-6.22, p = .000), whereas in controls, this effect was found in the placebo condition (2.90 vs. -1.14, respectively, 95% CI: 1.07-7.01, p = .010). In ASD, a similar pattern emerged when the learning target was social (3.00 vs. -0.64, respectively, 95% CI: -0.13 to 7.41, p = .057), whereas controls showed a reduced correlation for social learning targets under oxytocin (-0.70 vs. 2.72, respectively, 95% CI: -5.86 to 0.98, p = .008). The current data suggest that intranasal oxytocin has the potential to enhance social reinforcement learning in ASD. Future studies are warranted that investigate whether oxytocin can potentiate social learning when combined with behavioral therapies, resulting in greater treatment benefits than traditional behavior-only approaches.
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The influence of OXT was reflected in altered brain activity, manifested as an increased correlation in the reward prediction error signal within the NAc activation when social feedback was compared with non-social feedback.
“Moreover, the influence of OXT was reflected in altered brain activity, manifested as an increased correlation in the reward prediction error signal within the NAc activation when social feedback was compared with non-social feedback.”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Kruppa et al., 2019
The ROI analysis reports a higher correlation between the reward prediction error signal and left NAcc activation for social versus non-social feedback under OXT, but only in the ASD group. Healthy controls did not show that effect under OXT, so the claim omits an important population qualifier. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThis learning enhancement was specific to scenarios where the learning target and feedback were social, as opposed to non-social conditions.
“Interestingly, this learning enhancement was specific to scenarios where the learning target and feedback were social, as opposed to non-social conditions.”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Kruppa et al., 2019
The Abstract reports better learning under oxytocin in adults with ASD when either the target or the feedback was social, each compared with a non-social condition. But the Participants section says the study did not include a condition in which both the target and feedback were social, so it cannot establish enhancement in a scenario where both were social. Page numbers are not available in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measuredFunctional neuroimaging studies in persons with autism spectrum disorder have shown differences in regional brain activation in response to social stimuli after intranasal oxytocin, compared with placebo.
“These results have been supported by functional neuroimaging studies involving persons with autism spectrum disorder, which have shown differences in regional brain activation in response to social stimuli after the administration of intranasal oxytocin, as compared with placebo.11,15–17”
From Intranasal Oxytocin in Children and Adolescents with Autism Spectrum Disorder (2021) · cites this paper as [16]
Young individuals with ASD showed improved learning following intranasal OXT administration in a probabilistic reinforcement learning task.
“Young individuals with ASD showed improved learning following intranasal OXT administration in a prob abilistic reinforcement learning task (Kruppa et al., 2019).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Kruppa et al., 2019
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- Authors
- Kruppa, J. A., Gossen, A., Oberwelland Weiß, E., Kohls, G., Großheinrich, N., Cholemkery, H., Freitag, C. M., Karges, W., Wölfle, E., Sinzig, J., Fink, G. R., Herpertz-Dahlmann, B., Konrad, K., & Schulte-Rüther, M.
- Affiliations
- Forschungszentrum Jülich (DE)
- Universitätsklinikum Aachen (DE)
- Goethe University Frankfurt (DE)
- LVR-Klinik Bonn (DE)
- ORCID
- Venue
- Neuropsychopharmacology
- Published
- 2018-11-02
- Volume
- 44
- Issue
- 4
- Pages
- 749-756
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC6372686
- OpenAlex
- W2898648382
- Cited by
- 69
- References
- 44
- Citations by year
- 2026: 2 · 2025: 9 · 2024: 10 · 2023: 6 · 2022: 10 · 2021: 16 · 2020: 11 · 2019: 5
- FWCI
- 10.86
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
- JuSER (Forschungszentrum Jülich) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (FR2069/2-1)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- autism spectrum disorder, intranasal oxytocin, reward prediction error, nucleus accumbens, social motivation, social feedback, probabilistic reinforcement learning, computational modeling, placebo effect, adult male
- MeSH terms
- Social Learning, Autism Spectrum Disorder, Administration, Intranasal, Adolescent, Adult, Double-Blind Method, Humans, Magnetic Resonance Imaging, Male, Nucleus Accumbens, Oxytocin, Reinforcement, Social, Feedback, Psychological, Young Adult
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