Processing of social and monetary rewards in autism spectrum disorders

Sarah Baumeister; Carolin Moessnang; Nico Bast; Sarah Hohmann; Pascal Aggensteiner; Anna Kaiser; Julian Tillmann; David Goyard; Tony Charman; Sara Ambrosino; Simon Baron-Cohen; Christian Beckmann; Sven Bölte; Thomas Bourgeron; Annika Rausch; Daisy Crawley; Flavio Dell'Acqua; Guillaume Dumas; Sarah Durston; Christine Ecker; Dorothea L. Floris; Vincent Frouin; Hannah Hayward; Rosemary Holt; Mark H. Johnson; Emily J.H. Jones; Meng Chuan Lai; Michael V. Lombardo; Luke Mason; Bethany Oakley; Marianne Oldehinkel; Antonio M. Persico; Antonia San José Cáceres; Thomas Wolfers; Eva Loth; Declan G.M. Murphy; Jan K. Buitelaar; Heike Tost; Andreas Meyer-Lindenberg; Tobias Banaschewski; Daniel Brandeis

doi:10.1192/bjp.2022.157

Processing of social and monetary rewards in autism spectrum disorders

Sarah Baumeister^*, Carolin Moessnang, Nico Bast, Sarah Hohmann, Pascal Aggensteiner, Anna Kaiser, Julian Tillmann, David Goyard, Tony Charman, Sara Ambrosino, Simon Baron-Cohen, Christian Beckmann, Sven Bölte, Thomas Bourgeron, Annika Rausch, Daisy Crawley, Flavio Dell'Acqua, Guillaume Dumas, Sarah Durston, Christine EckerDorothea L. Floris, Vincent Frouin, Hannah Hayward, Rosemary Holt, Mark H. Johnson, Emily J.H. Jones, Meng Chuan Lai, Michael V. Lombardo, Luke Mason, Bethany Oakley, Marianne Oldehinkel, Antonio M. Persico, Antonia San José Cáceres, Thomas Wolfers, Eva Loth, Declan G.M. Murphy, Jan K. Buitelaar, Heike Tost, Andreas Meyer-Lindenberg, Tobias Banaschewski, Daniel Brandeis

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

8 Citations (Scopus)

Abstract

Background Reward processing has been proposed to underpin the atypical social feature of autism spectrum disorder (ASD). However, previous neuroimaging studies have yielded inconsistent results regarding the specificity of atypicalities for social reward processing in ASD. Aims Utilising a large sample, we aimed to assess reward processing in response to reward type (social, monetary) and reward phase (anticipation, delivery) in ASD. Method Functional magnetic resonance imaging during social and monetary reward anticipation and delivery was performed in 212 individuals with ASD (7.6-30.6 years of age) and 181 typically developing participants (7.6-30.8 years of age). Results Across social and monetary reward anticipation, whole-brain analyses showed hypoactivation of the right ventral striatum in participants with ASD compared with typically developing participants. Further, region of interest analysis across both reward types yielded ASD-related hypoactivation in both the left and right ventral striatum. Across delivery of social and monetary reward, hyperactivation of the ventral striatum in individuals with ASD did not survive correction for multiple comparisons. Dimensional analyses of autism and attention-deficit hyperactivity disorder (ADHD) scores were not significant. In categorical analyses, post hoc comparisons showed that ASD effects were most pronounced in participants with ASD without co-occurring ADHD. Conclusions Our results do not support current theories linking atypical social interaction in ASD to specific alterations in social reward processing. Instead, they point towards a generalised hypoactivity of ventral striatum in ASD during anticipation of both social and monetary rewards. We suggest this indicates attenuated reward seeking in ASD independent of social content and that elevated ADHD symptoms may attenuate altered reward seeking in ASD.

Original language	English
Pages (from-to)	100-111
Number of pages	12
Journal	British Journal of Psychiatry
Volume	222
Issue number	3
DOIs	https://doi.org/10.1192/bjp.2022.157
Publication status	Published - 29 Mar 2023

Keywords

ADHD symptoms
Autism spectrum disorder
autism traits
fMRI
multisite
reward processing

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10.1192/bjp.2022.157

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Baumeister, S., Moessnang, C., Bast, N., Hohmann, S., Aggensteiner, P., Kaiser, A., Tillmann, J., Goyard, D., Charman, T., Ambrosino, S., Baron-Cohen, S., Beckmann, C., Bölte, S., Bourgeron, T., Rausch, A., Crawley, D., Dell'Acqua, F., Dumas, G., Durston, S., ... Brandeis, D. (2023). Processing of social and monetary rewards in autism spectrum disorders. British Journal of Psychiatry, 222(3), 100-111. https://doi.org/10.1192/bjp.2022.157

@article{17fc34c4d0c9455f9c141dffd3ef553d,

title = "Processing of social and monetary rewards in autism spectrum disorders",

abstract = "Background Reward processing has been proposed to underpin the atypical social feature of autism spectrum disorder (ASD). However, previous neuroimaging studies have yielded inconsistent results regarding the specificity of atypicalities for social reward processing in ASD. Aims Utilising a large sample, we aimed to assess reward processing in response to reward type (social, monetary) and reward phase (anticipation, delivery) in ASD. Method Functional magnetic resonance imaging during social and monetary reward anticipation and delivery was performed in 212 individuals with ASD (7.6-30.6 years of age) and 181 typically developing participants (7.6-30.8 years of age). Results Across social and monetary reward anticipation, whole-brain analyses showed hypoactivation of the right ventral striatum in participants with ASD compared with typically developing participants. Further, region of interest analysis across both reward types yielded ASD-related hypoactivation in both the left and right ventral striatum. Across delivery of social and monetary reward, hyperactivation of the ventral striatum in individuals with ASD did not survive correction for multiple comparisons. Dimensional analyses of autism and attention-deficit hyperactivity disorder (ADHD) scores were not significant. In categorical analyses, post hoc comparisons showed that ASD effects were most pronounced in participants with ASD without co-occurring ADHD. Conclusions Our results do not support current theories linking atypical social interaction in ASD to specific alterations in social reward processing. Instead, they point towards a generalised hypoactivity of ventral striatum in ASD during anticipation of both social and monetary rewards. We suggest this indicates attenuated reward seeking in ASD independent of social content and that elevated ADHD symptoms may attenuate altered reward seeking in ASD.",

keywords = "ADHD symptoms, Autism spectrum disorder, autism traits, fMRI, multisite, reward processing",

author = "Sarah Baumeister and Carolin Moessnang and Nico Bast and Sarah Hohmann and Pascal Aggensteiner and Anna Kaiser and Julian Tillmann and David Goyard and Tony Charman and Sara Ambrosino and Simon Baron-Cohen and Christian Beckmann and Sven B{\"o}lte and Thomas Bourgeron and Annika Rausch and Daisy Crawley and Flavio Dell'Acqua and Guillaume Dumas and Sarah Durston and Christine Ecker and Floris, {Dorothea L.} and Vincent Frouin and Hannah Hayward and Rosemary Holt and Johnson, {Mark H.} and Jones, {Emily J.H.} and Lai, {Meng Chuan} and Lombardo, {Michael V.} and Luke Mason and Bethany Oakley and Marianne Oldehinkel and Persico, {Antonio M.} and {San Jos{\'e} C{\'a}ceres}, Antonia and Thomas Wolfers and Eva Loth and Murphy, {Declan G.M.} and Buitelaar, {Jan K.} and Heike Tost and Andreas Meyer-Lindenberg and Tobias Banaschewski and Daniel Brandeis",

note = "Funding Information: This work was supported by EU-AIMS (European Autism Interventions), which received support from the Innovative Medicines Initiative Joint Undertaking under grant agreement no. 115300, the resources of which are composed of financial contributions from the European Union{\textquoteright} s Seventh Framework Programme (grant FP7/2007-2013), from the European Federation of Pharmaceutical Industries and Associations companies{\textquoteright} in-kind contributions, and from Autism Speaks. The results leading to this publication have received funding from the Innovative Medicines Initiative 2 Joint Undertaking under grant agreement No 777394 for the project AIMS-2-TRIALS. This Joint Undertaking receives support from the European Union's Horizon 2020 research and innovation programme and EFPIA and AUTISM SPEAKS, Autistica, SFARI. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. Any views expressed are those of the author(s) and not necessarily those of the funders. Funding Information: A.M.L. has received consultant fees from Agence Nationale de la Recherche, Catania International Summer School of Neuroscience (CISSN), Daimler und Benz Stiftung, EPFL Brain Mind Institute, Fondation FondaMental, Hector Stiftung II, Invisio, Janssen-Cilag GmbH, Lundbeck A/S, Lundbeckfonden, Lundbeck Int. Neuroscience Foundation, MedinCell, Sage Therapeutics, Techspert.io, The LOOP Z{\"u}rich, University Medical Center Utrecht, University of Washington, von Behring R{\"o}ntgen Stiftung. He has received speaker fees from {\"A}rztekammer Nordrhein, BAG Psychiatrie Oberbayern, Biotest AG, Forum Werkstatt Karlsruhe, International Society of Psychiatric Genetics, Brentwood, Klinik f{\"u}r Psychiatrie und Psychotherapie Ingolstadt, Lundbeck SAS France, med Update GmbH, Merz-Stiftung, Siemens Healthineers, Society of Biological Psychiatry. A.M.L. has received editorial fees from American Association for the Advancement of Science, Elsevier, ECNP, Thieme Verlag and author fees from Thieme Verlag. D.M. has served on advisory boards for Roche and Servier, and has received research grants from Roche and J&J. W.M. has received lecture or travel fees from Pfizer, Gr{\"u}nenthal, University of Z{\"u}rich, International Association for the Study on Pain (IASP) and European Federation of IASP Chapters (EFIC). S.B. discloses that he has in the past 3 years acted as an author, consultant or lecturer for Medice and Roche. He receives royalties for textbooks and diagnostic tools from Huber/Hogrefe (German/Swedish versions of ADI-R, ADOS-2, SRS, SCQ), Kohlhammer and UTB. T.B. served in an advisory or consultancy role for ADHS digital, Infectopharm, Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, Roche, and Takeda. He received conference support or speaker's fee by Medice and Takeda. He received royalities from Hogrefe, Kohlhammer, CIP Medien, Oxford University Press. D.B. served as an unpaid scientific advisor for an EU-funded ADHD neurofeedback trial. A.S.J.C. received consultant fees and participated in several advisory boards from Roche and Servier. T.C. has received consultancy fees from Roche and Servier and royalties from SAGE Publications and Guilford Publications. J.K.B. has been in the past 3 years a consultant to/member of advisory board of/and/or speaker for Takeda/Shire, Roche, Medice, Angelini, Janssen, and Servier. He is not an employee of any of these companies, and not a stock shareholder of any of these companies. He has no other financial or material support, including expert testimony, patents, royalties. D.L.F. is supported by funding from the European Union's Horizon 2020 research and innovation programme under the Marie Sk{\l}odowska-Curie grant agreement No 101025785. All other authors report no potential conflict of interest. The present work is unrelated to the above grants and relationships. Publisher Copyright: Copyright {\textcopyright} The Author(s), 2023. Published by Cambridge University Press on behalf of the Royal College of Psychiatrists.",

year = "2023",

month = mar,

day = "29",

doi = "10.1192/bjp.2022.157",

language = "English",

volume = "222",

pages = "100--111",

journal = "British Journal of Psychiatry",

issn = "0007-1250",

publisher = "Cambridge University Press",

number = "3",

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Baumeister, S, Moessnang, C, Bast, N, Hohmann, S, Aggensteiner, P, Kaiser, A, Tillmann, J, Goyard, D, Charman, T, Ambrosino, S, Baron-Cohen, S, Beckmann, C, Bölte, S, Bourgeron, T, Rausch, A, Crawley, D , Dell'Acqua, F, Dumas, G, Durston, S, Ecker, C, Floris, DL, Frouin, V, Hayward, H, Holt, R, Johnson, MH, Jones, EJH, Lai, MC, Lombardo, MV, Mason, L, Oakley, B, Oldehinkel, M, Persico, AM, San José Cáceres, A, Wolfers, T, Loth, E , Murphy, DGM, Buitelaar, JK, Tost, H, Meyer-Lindenberg, A, Banaschewski, T & Brandeis, D 2023, 'Processing of social and monetary rewards in autism spectrum disorders', British Journal of Psychiatry, vol. 222, no. 3, pp. 100-111. https://doi.org/10.1192/bjp.2022.157

TY - JOUR

T1 - Processing of social and monetary rewards in autism spectrum disorders

AU - Baumeister, Sarah

AU - Moessnang, Carolin

AU - Bast, Nico

AU - Hohmann, Sarah

AU - Aggensteiner, Pascal

AU - Kaiser, Anna

AU - Tillmann, Julian

AU - Goyard, David

AU - Charman, Tony

AU - Ambrosino, Sara

AU - Baron-Cohen, Simon

AU - Beckmann, Christian

AU - Bölte, Sven

AU - Bourgeron, Thomas

AU - Rausch, Annika

AU - Crawley, Daisy

AU - Dell'Acqua, Flavio

AU - Dumas, Guillaume

AU - Durston, Sarah

AU - Ecker, Christine

AU - Floris, Dorothea L.

AU - Frouin, Vincent

AU - Hayward, Hannah

AU - Holt, Rosemary

AU - Johnson, Mark H.

AU - Jones, Emily J.H.

AU - Lai, Meng Chuan

AU - Lombardo, Michael V.

AU - Mason, Luke

AU - Oakley, Bethany

AU - Oldehinkel, Marianne

AU - Persico, Antonio M.

AU - San José Cáceres, Antonia

AU - Wolfers, Thomas

AU - Loth, Eva

AU - Murphy, Declan G.M.

AU - Buitelaar, Jan K.

AU - Tost, Heike

AU - Meyer-Lindenberg, Andreas

AU - Banaschewski, Tobias

AU - Brandeis, Daniel

N1 - Funding Information: This work was supported by EU-AIMS (European Autism Interventions), which received support from the Innovative Medicines Initiative Joint Undertaking under grant agreement no. 115300, the resources of which are composed of financial contributions from the European Union’ s Seventh Framework Programme (grant FP7/2007-2013), from the European Federation of Pharmaceutical Industries and Associations companies’ in-kind contributions, and from Autism Speaks. The results leading to this publication have received funding from the Innovative Medicines Initiative 2 Joint Undertaking under grant agreement No 777394 for the project AIMS-2-TRIALS. This Joint Undertaking receives support from the European Union's Horizon 2020 research and innovation programme and EFPIA and AUTISM SPEAKS, Autistica, SFARI. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. Any views expressed are those of the author(s) and not necessarily those of the funders. Funding Information: A.M.L. has received consultant fees from Agence Nationale de la Recherche, Catania International Summer School of Neuroscience (CISSN), Daimler und Benz Stiftung, EPFL Brain Mind Institute, Fondation FondaMental, Hector Stiftung II, Invisio, Janssen-Cilag GmbH, Lundbeck A/S, Lundbeckfonden, Lundbeck Int. Neuroscience Foundation, MedinCell, Sage Therapeutics, Techspert.io, The LOOP Zürich, University Medical Center Utrecht, University of Washington, von Behring Röntgen Stiftung. He has received speaker fees from Ärztekammer Nordrhein, BAG Psychiatrie Oberbayern, Biotest AG, Forum Werkstatt Karlsruhe, International Society of Psychiatric Genetics, Brentwood, Klinik für Psychiatrie und Psychotherapie Ingolstadt, Lundbeck SAS France, med Update GmbH, Merz-Stiftung, Siemens Healthineers, Society of Biological Psychiatry. A.M.L. has received editorial fees from American Association for the Advancement of Science, Elsevier, ECNP, Thieme Verlag and author fees from Thieme Verlag. D.M. has served on advisory boards for Roche and Servier, and has received research grants from Roche and J&J. W.M. has received lecture or travel fees from Pfizer, Grünenthal, University of Zürich, International Association for the Study on Pain (IASP) and European Federation of IASP Chapters (EFIC). S.B. discloses that he has in the past 3 years acted as an author, consultant or lecturer for Medice and Roche. He receives royalties for textbooks and diagnostic tools from Huber/Hogrefe (German/Swedish versions of ADI-R, ADOS-2, SRS, SCQ), Kohlhammer and UTB. T.B. served in an advisory or consultancy role for ADHS digital, Infectopharm, Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, Roche, and Takeda. He received conference support or speaker's fee by Medice and Takeda. He received royalities from Hogrefe, Kohlhammer, CIP Medien, Oxford University Press. D.B. served as an unpaid scientific advisor for an EU-funded ADHD neurofeedback trial. A.S.J.C. received consultant fees and participated in several advisory boards from Roche and Servier. T.C. has received consultancy fees from Roche and Servier and royalties from SAGE Publications and Guilford Publications. J.K.B. has been in the past 3 years a consultant to/member of advisory board of/and/or speaker for Takeda/Shire, Roche, Medice, Angelini, Janssen, and Servier. He is not an employee of any of these companies, and not a stock shareholder of any of these companies. He has no other financial or material support, including expert testimony, patents, royalties. D.L.F. is supported by funding from the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 101025785. All other authors report no potential conflict of interest. The present work is unrelated to the above grants and relationships. Publisher Copyright: Copyright © The Author(s), 2023. Published by Cambridge University Press on behalf of the Royal College of Psychiatrists.

PY - 2023/3/29

Y1 - 2023/3/29

N2 - Background Reward processing has been proposed to underpin the atypical social feature of autism spectrum disorder (ASD). However, previous neuroimaging studies have yielded inconsistent results regarding the specificity of atypicalities for social reward processing in ASD. Aims Utilising a large sample, we aimed to assess reward processing in response to reward type (social, monetary) and reward phase (anticipation, delivery) in ASD. Method Functional magnetic resonance imaging during social and monetary reward anticipation and delivery was performed in 212 individuals with ASD (7.6-30.6 years of age) and 181 typically developing participants (7.6-30.8 years of age). Results Across social and monetary reward anticipation, whole-brain analyses showed hypoactivation of the right ventral striatum in participants with ASD compared with typically developing participants. Further, region of interest analysis across both reward types yielded ASD-related hypoactivation in both the left and right ventral striatum. Across delivery of social and monetary reward, hyperactivation of the ventral striatum in individuals with ASD did not survive correction for multiple comparisons. Dimensional analyses of autism and attention-deficit hyperactivity disorder (ADHD) scores were not significant. In categorical analyses, post hoc comparisons showed that ASD effects were most pronounced in participants with ASD without co-occurring ADHD. Conclusions Our results do not support current theories linking atypical social interaction in ASD to specific alterations in social reward processing. Instead, they point towards a generalised hypoactivity of ventral striatum in ASD during anticipation of both social and monetary rewards. We suggest this indicates attenuated reward seeking in ASD independent of social content and that elevated ADHD symptoms may attenuate altered reward seeking in ASD.

AB - Background Reward processing has been proposed to underpin the atypical social feature of autism spectrum disorder (ASD). However, previous neuroimaging studies have yielded inconsistent results regarding the specificity of atypicalities for social reward processing in ASD. Aims Utilising a large sample, we aimed to assess reward processing in response to reward type (social, monetary) and reward phase (anticipation, delivery) in ASD. Method Functional magnetic resonance imaging during social and monetary reward anticipation and delivery was performed in 212 individuals with ASD (7.6-30.6 years of age) and 181 typically developing participants (7.6-30.8 years of age). Results Across social and monetary reward anticipation, whole-brain analyses showed hypoactivation of the right ventral striatum in participants with ASD compared with typically developing participants. Further, region of interest analysis across both reward types yielded ASD-related hypoactivation in both the left and right ventral striatum. Across delivery of social and monetary reward, hyperactivation of the ventral striatum in individuals with ASD did not survive correction for multiple comparisons. Dimensional analyses of autism and attention-deficit hyperactivity disorder (ADHD) scores were not significant. In categorical analyses, post hoc comparisons showed that ASD effects were most pronounced in participants with ASD without co-occurring ADHD. Conclusions Our results do not support current theories linking atypical social interaction in ASD to specific alterations in social reward processing. Instead, they point towards a generalised hypoactivity of ventral striatum in ASD during anticipation of both social and monetary rewards. We suggest this indicates attenuated reward seeking in ASD independent of social content and that elevated ADHD symptoms may attenuate altered reward seeking in ASD.

KW - ADHD symptoms

KW - Autism spectrum disorder

KW - autism traits

KW - fMRI

KW - multisite

KW - reward processing

UR - http://www.scopus.com/inward/record.url?scp=85148113099&partnerID=8YFLogxK

U2 - 10.1192/bjp.2022.157

DO - 10.1192/bjp.2022.157

M3 - Article

C2 - 36700346

AN - SCOPUS:85148113099

SN - 0007-1250

VL - 222

SP - 100

EP - 111

JO - British Journal of Psychiatry

JF - British Journal of Psychiatry

IS - 3

ER -

Processing of social and monetary rewards in autism spectrum disorders

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