Mapping social reward and punishment processing in the human brain: A voxel-based meta-analysis of neuroimaging findings using the social incentive delay task
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Abstract
Social rewards or punishments motivate human learning and behaviour, and alterations in the brain circuits involved in the processing of these stimuli have been linked with several neuropsychiatric disorders. However, questions still remain about the exact neural substrates implicated in social reward and punishment processing. Here, we conducted four Anisotropic Effect Size Signed Differential Mapping voxel-based meta-analyses of fMRI studies investigating the neural correlates of the anticipation and receipt of social rewards and punishments using the Social Incentive Delay task. We found that the anticipation of both social rewards and social punishment avoidance recruits a wide network of areas including the basal ganglia, the midbrain, the dorsal anterior cingulate cortex, the supplementary motor area, the anterior insula, the occipital gyrus and other frontal, temporal, parietal and cerebellar regions not captured in previous coordinate-based meta-analysis. We identified decreases in the BOLD signal during the anticipation of both social reward and punishment avoidance in regions of the default-mode network that were missed in individual studies likely due to a lack of power. Receipt of social rewards engaged a robust network of brain regions including the ventromedial frontal and orbitofrontal cortices, the anterior cingulate cortex, the amygdala, the hippocampus, the occipital cortex and the brainstem, but not the basal ganglia. Receipt of social punishments increased the BOLD signal in the orbitofrontal cortex, superior and inferior frontal gyri, lateral occipital cortex and the insula. In contrast to the receipt of social rewards, we also observed a decrease in the BOLD signal in the basal ganglia in response to the receipt of social punishments. Our results provide a better understanding of the brain circuitry involved in the processing of social rewards and punishment. Furthermore, they can inform hypotheses regarding brain areas where disruption in activity may be associated with dysfunctional social incentive processing during disease.
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The positive valence system supports social bond formation and maintenance.
“These positive valence processes create a cycle supporting the initiation and strengthening of social bonds regulated by the mesolimbic reward circuit that activates in response to cues signaling potential social reward(16–18) (i.e., incentive salience or ‘wanting’).(19)”
Positive valence processes create a cycle supporting the initiation and strengthening of social bonds regulated by the mesolimbic reward circuit that activates in response to cues signaling potential social reward.
“These positive valence processes create a cycle supporting the initiation and strengthening of social bonds regulated by the mesolimbic reward circuit that activates in response to cues signaling potential social reward(16–18) (i.e., incentive salience or ‘wanting’).(19)”
The Social Incentive Delay task reliably activates the striatum when people anticipate obtaining social rewards.
“The SID(52) reliably activates the striatum (primary region of interest) when people anticipate obtaining social rewards (e.g., viewing a smiling face).(18)”
Social reward processing is multifaceted, involving different phases (e.g., anticipation, responsiveness) and brain regions outside of the striatum (e.g., anterior insula, anterior cingulate cortex).
“social reward processing is multifaceted, involving different phases (e.g., anticipation, responsiveness) and brain regions outside of the striatum (e.g., anterior insula, anterior cingulate cortex).(18)”
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Vanova, M., Aldridge‐Waddon, L., Puzzo, I., & Kumari, V. (2025) · Brain and Behavior · doi:10.1002/brb3.70776
Cheng, C. C. C., Tsang, H. L. M., Han, M., Zhang, J., Maes, M. H. J., Klugah‐Brown, B., Bore, M. C., & Becker, B. (2025) · medRxiv · doi:10.1101/2025.04.06.25325353 · Cited by 1 · see citing works
Zhou, X., Xu, T., Zeng, Y., Zhang, R., Qi, Z., Zhao, W., Kendrick, K. M., & Becker, B. (2021) · doi:10.22541/au.163251473.31756493/v1
The Basal Forebrain Serves Social Information ProcessingPreprint
Sobczak, A., & Bunzeck, N. (2023) · doi:10.31219/osf.io/juqpr
The basal forebrain serves social information processing
Sobczak, A., & Bunzeck, N. (2024) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2024.101372
What do hippocampal cell fields represent?
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0007
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0001
The neurology of anxiety—planning circuits
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0011
A theory of the septo-hippocampal system (SHS)
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0010
Symptoms and syndromes of anxiety
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0013
The neurology of anxiety—survival circuits
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0006
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0002
The treatment of anxiety and fear disorders
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0014
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0011
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0015
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0009
The anxiolytic drugs—our key tool
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0004
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0003
List of online appendices and reviews
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0010
A conceptual theory of the goal inhibition system
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0005
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0006
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0004
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0005
Do, K. T., Paolizzi, S. G., & Hallquist, M. N. (2024) · doi:10.31234/osf.io/nrm9f
Dissociable neurofunctional and molecular characterizations of reward and punishment sensitivityPreprint
Xu, T., Zhu, C., Zhou, X., Chen, Z., Gan, X., Cui, X., Zhou, F., Zhang, R., Zhao, W., Zhang, X., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.12.30.630747
- Authors
- Martins, D., Rademacher, L., Gabay, A. S., Taylor, R., Richey, J. A., Smith, D. V., Goerlich, K. S., Nawijn, L., Cremers, H. R., Wilson, R., Bhattacharyya, S., & Paloyelis, Y.
- Affiliations
- King's College London (GB)
- Goethe University Frankfurt (DE)
- University of Oxford (GB)
- Virginia Tech (US)
- Temple University (US)
- University Medical Center Groningen (NL)
- Amsterdam Neuroscience (NL)
- University of Amsterdam (NL)
- Corresponding author
- Martins, D.
- ORCID
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 2021-03
- Volume
- 122
- Pages
- 1-17
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W3119461430
- Cited by
- 119
- References
- 123
- Citations by year
- 2026: 15 · 2025: 20 · 2024: 43 · 2023: 16 · 2022: 12 · 2021: 13
- FWCI
- 3.07
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, cc-by)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (acceptedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Research Portal (King's College London) (submittedVersion, cc-by-nc-nd)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Economic and Social Research Council
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- social reward, social punishment, reward anticipation, punishment avoidance, neural correlates, default mode network, basal ganglia, orbitofrontal cortex, anterior cingulate cortex, amygdala, supplementary motor area, anterior insula, neuropsychiatric disorders
- MeSH terms
- Brain, Brain Mapping, Humans, Magnetic Resonance Imaging, Motivation, Punishment, Reward, Neuroimaging
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