Assessment of Reward-Related Brain Function After a Single Dose of Oxytocin in Autism: A Randomized Controlled Trial

Annalina V. Mayer; Katrin Preckel; Kristin Ihle; Fabian A. Piecha; Klaus Junghanns; Stefan Reiche; Lena Rademacher; Laura Müller-Pinzler; David S. Stolz; Inge Kamp-Becker; Sanna Stroth; Stefan Roepke; Charlotte Küpper; Veronika Engert; Tania Singer; Philipp Kanske; Frieder M. Paulus; Sören Krach

doi:10.1016/j.bpsgos.2021.10.004

Assessment of Reward-Related Brain Function After a Single Dose of Oxytocin in Autism: A Randomized Controlled Trial

Annalina V. Mayer^*, Katrin Preckel, Kristin Ihle, Fabian A. Piecha, Klaus Junghanns, Stefan Reiche, Lena Rademacher, Laura Müller-Pinzler, David S. Stolz, Inge Kamp-Becker, Sanna Stroth, Stefan Roepke, Charlotte Küpper, Veronika Engert, Tania Singer, Philipp Kanske, Frieder M. Paulus, Sören Krach

^*Corresponding author for this work

7 Citations (Scopus)

Abstract

Background: Autism spectrum disorder (ASD) is characterized by difficulties in social communication and interaction, which have been related to atypical neural processing of rewards, especially in the social domain. As intranasal oxytocin has been shown to modulate activation of the brain's reward circuit, oxytocin might ameliorate the processing of social rewards in ASD and thus improve social difficulties. Methods: In this randomized, double-blind, placebo-controlled, crossover functional magnetic resonance imaging study, we examined effects of a 24-IU dose of intranasal oxytocin on reward-related brain function in 37 men with ASD without intellectual impairment and 37 age- and IQ-matched control participants. Participants performed an incentive delay task that allows the investigation of neural activity associated with the anticipation and receipt of monetary and social rewards. Results: Nonsignificant tests suggested that oxytocin did not influence neural processes related to the anticipation of social or monetary rewards in either group. Complementary Bayesian analyses indicated moderate evidence for a null model, relative to an alternative model. Our results were inconclusive regarding possible oxytocin effects on amygdala responsiveness to social rewards during reward consumption. There were no significant differences in reward-related brain function between the two groups under placebo. Conclusions: Our results do not support the hypothesis that intranasal oxytocin generally enhances activation of reward-related neural circuits in men with and without ASD.

Original language	English
Journal	Biological Psychiatry Global Open Science
Volume	2
Issue number	2
Pages (from-to)	136-146
Number of pages	11
DOIs	https://doi.org/10.1016/j.bpsgos.2021.10.004
Publication status	Published - 04.2022

Funding

This clinical trial was part of the ASD-Net, the German consortium for Autism Spectrum Disorder, and was funded by the German Federal Ministry of Education and Research (Grant Nos. 01EE1409H and 01EE1409I; funding period: 2015–2019). Parts of the study were performed and MRI data were assessed at the former Department of Social Neuroscience at the Max Planck Institute for Human Cognitive and Brain Sciences Leipzig headed by TS until 2018. Funding required for neuroimaging, the support team (e.g. technical, imaging, physician, recruitment), and some of the researchers (PK and VE) during that period was provided by the Max Planck Society as TS's budget she received as director of the Department of Social Neuroscience. We acknowledge financial support by Land Schleswig-Holstein within the funding programme Open Access Publikationsfonds. We thank Johanna Klose, Kerstin Neubauer, Franca Schwesinger, Katharina Ohm, Sarah Rösch, and Lisa Nix for their help as student assistants; Janine Baumann, Nora Czekalla, Jöran Lepsien, Toralf Mildner, André Pampel, Manuela Hofmann, Sylvie Neubert, Mandy Jochemko, Anke Kummer, Simone Wipper, Nicole Pampus, and Domenica Klank for assistance in neuroimaging; Martin Göttlich for assistance in data analysis; Norbert Brüggemann, Henrike Hanßen, and Anna Kosatschek for their assistance as study physicians; Natalia Chechko, Susanne Stickel (Aachen), Gerti Gerber (Marburg), Daniel Alvarez-Fischer, Veronika Thorns (Lübeck), Stefan Ehrlich, and Veit Rössner (Dresden) for their efforts during participant recruitment; Henrik Grunert and Kerstin Traeger for technical assistance; Matthias Collier, Kathrin Scheibe, and Silke Hauer from the Clinical Trial Centre Leipzig for providing data management tools and randomization; and Anne-Kathrin Wermter for her kind assistance during the preparation of this study. A previous version of this article was published as a preprint on MedRxiv: https://doi.org/10.1101/2021.03.19.21253900. The authors report no biomedical financial interests or potential conflicts of interest.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being
SDG 5 Gender Equality
SDG 10 Reduced Inequalities

Research Areas and Centers

Academic Focus: Center for Brain, Behavior and Metabolism (CBBM)

DFG Research Classification Scheme

2.23-08 Human Cognitive and Systems Neuroscience

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10.1016/j.bpsgos.2021.10.004

Cite this

Mayer, A. V., Preckel, K., Ihle, K., Piecha, F. A., Junghanns, K., Reiche, S., Rademacher, L., Müller-Pinzler, L., Stolz, D. S., Kamp-Becker, I., Stroth, S., Roepke, S., Küpper, C., Engert, V., Singer, T., Kanske, P., Paulus, F. M., & Krach, S. (2022). Assessment of Reward-Related Brain Function After a Single Dose of Oxytocin in Autism: A Randomized Controlled Trial. Biological Psychiatry Global Open Science, 2(2), 136-146. https://doi.org/10.1016/j.bpsgos.2021.10.004

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title = "Assessment of Reward-Related Brain Function After a Single Dose of Oxytocin in Autism: A Randomized Controlled Trial",

abstract = "Background: Autism spectrum disorder (ASD) is characterized by difficulties in social communication and interaction, which have been related to atypical neural processing of rewards, especially in the social domain. As intranasal oxytocin has been shown to modulate activation of the brain's reward circuit, oxytocin might ameliorate the processing of social rewards in ASD and thus improve social difficulties. Methods: In this randomized, double-blind, placebo-controlled, crossover functional magnetic resonance imaging study, we examined effects of a 24-IU dose of intranasal oxytocin on reward-related brain function in 37 men with ASD without intellectual impairment and 37 age- and IQ-matched control participants. Participants performed an incentive delay task that allows the investigation of neural activity associated with the anticipation and receipt of monetary and social rewards. Results: Nonsignificant tests suggested that oxytocin did not influence neural processes related to the anticipation of social or monetary rewards in either group. Complementary Bayesian analyses indicated moderate evidence for a null model, relative to an alternative model. Our results were inconclusive regarding possible oxytocin effects on amygdala responsiveness to social rewards during reward consumption. There were no significant differences in reward-related brain function between the two groups under placebo. Conclusions: Our results do not support the hypothesis that intranasal oxytocin generally enhances activation of reward-related neural circuits in men with and without ASD.",

author = "Mayer, \{Annalina V.\} and Katrin Preckel and Kristin Ihle and Piecha, \{Fabian A.\} and Klaus Junghanns and Stefan Reiche and Lena Rademacher and Laura M{\"u}ller-Pinzler and Stolz, \{David S.\} and Inge Kamp-Becker and Sanna Stroth and Stefan Roepke and Charlotte K{\"u}pper and Veronika Engert and Tania Singer and Philipp Kanske and Paulus, \{Frieder M.\} and S{\"o}ren Krach",

note = "Publisher Copyright: {\textcopyright} 2021 The Authors",

year = "2022",

month = apr,

doi = "10.1016/j.bpsgos.2021.10.004",

language = "English",

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Mayer, AV, Preckel, K, Ihle, K, Piecha, FA, Junghanns, K, Reiche, S, Rademacher, L , Müller-Pinzler, L , Stolz, DS, Kamp-Becker, I, Stroth, S, Roepke, S, Küpper, C, Engert, V, Singer, T, Kanske, P, Paulus, FM & Krach, S 2022, 'Assessment of Reward-Related Brain Function After a Single Dose of Oxytocin in Autism: A Randomized Controlled Trial', Biological Psychiatry Global Open Science, vol. 2, no. 2, pp. 136-146. https://doi.org/10.1016/j.bpsgos.2021.10.004

TY - JOUR

T1 - Assessment of Reward-Related Brain Function After a Single Dose of Oxytocin in Autism

T2 - A Randomized Controlled Trial

AU - Mayer, Annalina V.

AU - Preckel, Katrin

AU - Ihle, Kristin

AU - Piecha, Fabian A.

AU - Junghanns, Klaus

AU - Reiche, Stefan

AU - Rademacher, Lena

AU - Müller-Pinzler, Laura

AU - Stolz, David S.

AU - Kamp-Becker, Inge

AU - Stroth, Sanna

AU - Roepke, Stefan

AU - Küpper, Charlotte

AU - Engert, Veronika

AU - Singer, Tania

AU - Kanske, Philipp

AU - Paulus, Frieder M.

AU - Krach, Sören

PY - 2022/4

Y1 - 2022/4

N2 - Background: Autism spectrum disorder (ASD) is characterized by difficulties in social communication and interaction, which have been related to atypical neural processing of rewards, especially in the social domain. As intranasal oxytocin has been shown to modulate activation of the brain's reward circuit, oxytocin might ameliorate the processing of social rewards in ASD and thus improve social difficulties. Methods: In this randomized, double-blind, placebo-controlled, crossover functional magnetic resonance imaging study, we examined effects of a 24-IU dose of intranasal oxytocin on reward-related brain function in 37 men with ASD without intellectual impairment and 37 age- and IQ-matched control participants. Participants performed an incentive delay task that allows the investigation of neural activity associated with the anticipation and receipt of monetary and social rewards. Results: Nonsignificant tests suggested that oxytocin did not influence neural processes related to the anticipation of social or monetary rewards in either group. Complementary Bayesian analyses indicated moderate evidence for a null model, relative to an alternative model. Our results were inconclusive regarding possible oxytocin effects on amygdala responsiveness to social rewards during reward consumption. There were no significant differences in reward-related brain function between the two groups under placebo. Conclusions: Our results do not support the hypothesis that intranasal oxytocin generally enhances activation of reward-related neural circuits in men with and without ASD.

AB - Background: Autism spectrum disorder (ASD) is characterized by difficulties in social communication and interaction, which have been related to atypical neural processing of rewards, especially in the social domain. As intranasal oxytocin has been shown to modulate activation of the brain's reward circuit, oxytocin might ameliorate the processing of social rewards in ASD and thus improve social difficulties. Methods: In this randomized, double-blind, placebo-controlled, crossover functional magnetic resonance imaging study, we examined effects of a 24-IU dose of intranasal oxytocin on reward-related brain function in 37 men with ASD without intellectual impairment and 37 age- and IQ-matched control participants. Participants performed an incentive delay task that allows the investigation of neural activity associated with the anticipation and receipt of monetary and social rewards. Results: Nonsignificant tests suggested that oxytocin did not influence neural processes related to the anticipation of social or monetary rewards in either group. Complementary Bayesian analyses indicated moderate evidence for a null model, relative to an alternative model. Our results were inconclusive regarding possible oxytocin effects on amygdala responsiveness to social rewards during reward consumption. There were no significant differences in reward-related brain function between the two groups under placebo. Conclusions: Our results do not support the hypothesis that intranasal oxytocin generally enhances activation of reward-related neural circuits in men with and without ASD.

UR - https://www.scopus.com/pages/publications/85148560684

U2 - 10.1016/j.bpsgos.2021.10.004

DO - 10.1016/j.bpsgos.2021.10.004

M3 - Comments/Debates

AN - SCOPUS:85148560684

SN - 2667-1743

VL - 2

SP - 136

EP - 146

JO - Biological Psychiatry Global Open Science

JF - Biological Psychiatry Global Open Science

IS - 2

ER -

Assessment of Reward-Related Brain Function After a Single Dose of Oxytocin in Autism: A Randomized Controlled Trial

Abstract

Funding

UN SDGs

Research Areas and Centers

DFG Research Classification Scheme

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