Reward processing in autism
Open accessAbstract
The social motivation hypothesis of autism posits that infants with autism do not experience social stimuli as rewarding, thereby leading to a cascade of potentially negative consequences for later development. While possible downstream effects of this hypothesis such as altered face and voice processing have been examined, there has not been a direct investigation of social reward processing in autism. Here we use functional magnetic resonance imaging to examine social and monetary rewarded implicit learning in children with and without autism spectrum disorders (ASD). Sixteen males with ASD and sixteen age‐ and IQ‐matched typically developing (TD) males were scanned while performing two versions of a rewarded implicit learning task. In addition to examining responses to reward, we investigated the neural circuitry supporting rewarded learning and the relationship between these factors and social development. We found diminished neural responses to both social and monetary rewards in ASD, with a pronounced reduction in response to social rewards (SR). Children with ASD also demonstrated a further deficit in frontostriatal response during social, but not monetary, rewarded learning. Moreover, we show a relationship between ventral striatum activity and social reciprocity in TD children. Together, these data support the hypothesis that children with ASD have diminished neural responses to SR, and that this deficit relates to social learning impairments.
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Scott-Van Zeeland et al. found diminished ventral striatal response during social-reward outcomes and also, but to a lesser extent, with monetary-reward outcomes in children with ASDs.
“They found diminished ventral striatal response during social-reward outcomes and also, but to a lesser extent, with monetary-reward outcomes.”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [564]
Activity within the ventral striatum predicted social reciprocity within the control group but not the ASD group.
“Activity within the ventral striatum was found to predict social reciprocity within the control group but not the ASD group.”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [564]
The orbitofrontal-striatum-amygdala circuit is abnormal in ASD, particularly in response to social stimuli such as faces, social approval, or social rejection.
“The orbitofrontal–striatum-amygdala circuit has been repeatedly highlighted as abnormal in ASD[76], in particular in response to social stimuli such as faces [77], social approval [78], or social rejection [79].”
From The social motivation theory of autism (2012) · cites this paper as [78]
Few neuroimaging studies have directly addressed social versus non-social reward processing in ASD, and findings to date have not been entirely consistent.
“only few neuroimaging studies have directly addressed the basis of social vs. non-social reward processing in ASD and findings to date have not been entirely consistent (perhaps, in part, due to the lack of potent social reward paradigms) [78,80]”
From The social motivation theory of autism (2012) · cites this paper as [78]
Lowering the threshold to an uncorrected voxel height of p < 0.005 with an extent cluster size of at least 20 voxels, the ASD group, compared to TDC and ADHD, showed diminished activation in ventral striatum in response to monetary reward.
“However, lowering the threshold to an uncorrected voxel height of p < 0.005 with an extent cluster size of at least 20 voxels (according to Scott-Van Zeeland et al., 2010), which still produces desirable balance between Types I and II errors comparable to false discovery rate (Lieberman and Cunningham, 2009), the ASD group, compared to TDC and ADHD, showed diminished activation in ventral striatum”
From Differentiating neural reward responsiveness in autism versus ADHD (2014) · cites this paper as Scott-Van Zeeland et al., 2010
We did not find greater malfunctions in the reward circuitry in response to social reward compared to monetary reward in children with ASD.
“It should be pointed out that we did not find greater malfunctions in the reward circuitry in response to social reward compared to monetary reward in children with ASD (Delmonte et al., 2012, Scott-Van Zeeland et al., 2010).”
From Differentiating neural reward responsiveness in autism versus ADHD (2014) · cites this paper as Scott-Van Zeeland et al., 2010
Low ventral striatum activation in ASD further emphasizes recent imaging findings of reward circuitry dysfunction in ASD not only in response to social rewards but also for tangible rewards like money.
“Low ventral striatum activation in ASD further emphasizes recent imaging findings of reward circuitry dysfunction in ASD not only in response to social rewards (Delmonte et al., 2012, Scott-Van Zeeland et al., 2010), but also for tangible rewards like money (Dichter et al., 2012c, Dichter et al., 2012b, Kohls et al., 2011, Kohls et al., 2013b, Richey et al., 2012, Schmitz et al., 2008).”
From Differentiating neural reward responsiveness in autism versus ADHD (2014) · cites this paper as Scott-Van Zeeland et al., 2010
In Scott-Van Zeeland et al., the ASD group displayed diminished VS activation for social reward, but not for monetary reward.
“In this study, the ASD group displayed diminished activation in the VS for social reward, but not for monetary reward.”
From Social “wanting” dysfunction in autism: neurobiological underpinnings and treatment implications (2012) · cites this paper as [62]
In Scott-Van Zeeland et al., VS activation to social reward predicted social capacities within the TDC group, but not the ASD group.
“In addition, VS activation to social reward predicted social capacities (as measured by the Social Responsiveness Scale) within the TDC group, but not the ASD group.”
From Social “wanting” dysfunction in autism: neurobiological underpinnings and treatment implications (2012) · cites this paper as [62]
Four out of five published fMRI studies reported diminished VS activation in individuals with ASD compared with TDC when processing either social or monetary reward versus non-reward.
“Four out of five published fMRI studies reported diminished VS activation in individuals with ASD compared with TDC when processing either social or monetary reward versus non-reward [30,60-62].”
From Social “wanting” dysfunction in autism: neurobiological underpinnings and treatment implications (2012) · cites this paper as [62]
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SHANK3 controls maturation of social reward circuits in the VTA
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Brief Report: Selective Social Anhedonia in High Functioning Autism
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From early markers to neuro-developmental mechanisms of autism
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Empathy in autism Spectrum disorder
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Reputation Management: Evidence for Ability But Reduced Propensity in Autism
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Self-citationCarlisi, C. O., Norman, L., Murphy, C. M., Christakou, A., Chantiluke, K., Giampietro, V., Simmons, A., Brammer, M., Murphy, D. G., MRC AIMS consortium, et al. (2017) · Psychological Medicine · doi:10.1017/s0033291717001088 · Cited by 49 · see citing works
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“There is also support for the social motivation hypothesis from neuroimaging studies: individuals with ASD have shown reduced neural activation in frontostriatal regions implicated in reward processing during social reward tasks relative to typically developing controls (reward anticipation: [10]; receipt: [11]; learn…”
ResultAdditive effects of oxytocin receptor gene polymorphisms on reward circuitry in youth with autism
Hernandez, L. M., Krasileva, K., Green, S. A., Sherman, L. E., Ponting, C., McCarron, R., Lowe, J. K., Geschwind, D. H., Bookheimer, S. Y., & Dapretto, M. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.209 · Cited by 43 · see citing works
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The sociability spectrum: evidence from reciprocal genetic copy number variations
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An update on the neurobiology of repetitive behaviors in autism
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- Authors
- Scott‐Van Zeeland, A. A., Dapretto, M., Ghahremani, D. G., Poldrack, R. A., & Bookheimer, S. Y.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Bookheimer, Susan Y.
- Venue
- Autism Research
- Publisher
- Wiley
- Published
- 2010-03-31
- Volume
- 3
- Issue
- 2
- Pages
- 53-67
- ISSN
- 1939-3792 (ISSN-L)
- 1939-3806
- PMC
- PMC3076289
- OpenAlex
- W2087480671
- Cited by
- 458
- References
- 62
- Citations by year
- 2026: 14 · 2025: 25 · 2024: 19 · 2023: 34 · 2022: 22 · 2021: 30 · 2020: 38 · 2019: 32 · 2018: 42 · 2017: 27 · 2016: 36 · 2015: 34 · 2014: 32 · 2013: 32 · 2012: 26
- FWCI
- 14.12
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Autism Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Autism Speaks (AS1626)
- National Institute of Mental Health (F31MH079645, T32MH073526)
- National Center for Research Resources (P41RR013642, RR 13642, RR00865, M01RR000865, UL1RR025774, C06RR012169)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P0I HD035470, P01HD035470, P50HD055784, R01HD065280)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- autism spectrum disorder, social reward processing, monetary rewards, implicit learning, ventral striatum, frontostriatal circuits, social reciprocity, children
- MeSH terms
- Adult, Autistic Disorder, Brain, Cognition Disorders, Female, Humans, Learning, Magnetic Resonance Imaging, Male, Middle Aged, Neuropsychological Tests, Reward, Severity of Illness Index, Social Perception
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