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The Neural Substrates of Reward Processing in Humans: The Modern Role of fMRI
Abstract
Experimental work in animals has identified numerous neural structures involved in reward processing and reward-dependent learning. Until recently, this work provided the primary basis for speculations about the neural substrates of human reward processing. The widespread use of neuroimaging technology has changed this situation dramatically over the past decade through the use of PET and fMRI. Here, the authors focus on the role played by fMRI studies, where recent work has replicated the animal results in human subjects and has extended the view of putative reward-processing neural structures. In particular, fMRI work has identified a set of reward-related brain structures including the orbitofrontal cortex, amygdala, ventral striatum, and medial prefrontal cortex. Moreover, the human experiments have probed the dependence of human reward responses on learned expectations, context, timing, and the reward dimension. Current experiments aim to assess the function of human reward-processing structures to determine how they allow us to predict, assess, and act in response to rewards. The authors review current accomplishments in the study of human reward processing and focus their discussion on explanations directed particularly at the role played by the ventral striatum. They discuss how these findings may contribute to a better understanding of deficits associated with Parkinson’s disease.
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“The ventral striatum has been implicated in reward-related processing in humans (Knutson, Adams, Fong, & Hommer, 2001; McClure, York, & Montague, 2004) and animals (Elliott, Friston, & Dolan, 2000).”
From Gender Differences in Emotion Regulation: An fMRI Study of Cognitive Reappraisal (2008) · cites this paper as McClure, York, & Montague, 2004
In the citing paper
“and may underlie bias for immediate over future rewards (McClure et al., 2004).”
From Developmental changes in brain function underlying the influence of reward processing on inhibitory control (2011) · cites this paper as McClure et al., 2004
In the citing paper
“The adult literature using such paradigms has shown that the striatum is sensitive to (monetary) rewards (Breiter et al., 2001; Delgado, 2007; McClure et al., 2004).”
From Testosterone levels correspond with increased ventral striatum activation in response to monetary rewards in adolescents (2011) · cites this paper as McClure et al., 2004
In the citing paper
“it has not yet been confirmed that, across studies, adolescents reliably activate the same regions during reward based processing as do adults (McClure et al., 2004; Liu et al., 2011; Bartra et al., 2013).”
From Neural networks involved in adolescent reward processing: an activation likelihood estimation meta-analysis of functional neuroimaging studies (2015) · cites this paper as McClure et al., 2004
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BackgroundHumans Integrate Monetary and Liquid Incentives to Motivate Cognitive Task Performance
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Neural response to pictorial health warning labels can predict smoking behavioral change
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“, 2008), and is a region more generally implicated in reward and motivation (Haber and Knutson, 2009; Knutson and Cooper, 2005; McClure et al., 2004).”
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“Both of these subcortical results are consistent with previous findings of reward processing in RL-related circuits (Delgado et al. 2000; McClure et al. 2004; Foerde and Shohamy 2011; Li et al. 2011; Davidow et al. 2016; Palombo et al. 2019).”
ResultWinning is not enough: ventral striatum connectivity during physical aggression
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“However, certain brain areas are consistently associated with reward processing in healthy humans: striatum (nucleus accumbens, nucleus caudatus, putamen), orbitofrontal cortex, anterior cingulate gyrus and other parts of the prefrontal cortex (McClure et al., 2004).”
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“In such systems, adding information from more frontal electrodes may be able to provide an increase in classification accuracy, as the frontal cortex has been shown to code prediction and reward (Schultz et al., 1997; Schultz, 2001; McClure et al., 2004).”
BackgroundValue, drug addiction and the brain
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Independent circuits in basal ganglia and cortex for the processing of reward and precision feedback
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“Decades of neurophysiological and neuroimaging studies have demonstrated that the meso-corticostriatal pathway is central to this function (McClure et al., 2004; O'Doherty, 2004; Schultz, 2000, 2006, 2013).”
ResultRelationship between Personality Traits and Brain Reward Responses when Playing on a Team
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“…and have established the vmPFC as a key component in the reward circuitry. vmPFC activity has been linked to a wide range of valuation and choice signals [60] and to value-guided decision-making by monitoring and evaluating reward outcomes [61], including both social and monetary rewards [54].”
BackgroundResultCost-benefit analysis: the first real rule of fight club?
Hillman, K. L. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00248 · Cited by 17
“BOLD activity in the ventral striatum and OFC correlate to self-reports of schadenfreude (McClure et al., 2004; Fehr and Camerer, 2007; Takahashi et al., 2009), and activity in the dorsal ACC to self-reports of envy (Takahashi et al., 2009).”
BackgroundRewarding images do not invoke the reward positivity: They inflate it
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“, 2009), striatum (Cromwell et al., 2005; Delgado et al., 2000; Izuma et al., 2008; McClure et al., 2004; O’Doherty et al., 2004; Schultz et al., 2000), and cortex (Gehring and Willoughby, 2002; Rogers et al.”
BackgroundLevodopa and the feedback process on set‐shifting in parkinson's disease
Au, W. L., Zhou, J. H., Palmes, P., Sitoh, Y., Tan, L., & Rajapakse, J. C. (2011) · Human Brain Mapping · doi:10.1002/hbm.21187 · Cited by 16
“These cognitive functions are dependent on the proper functioning of the striatum and its dopaminergic projections [Holroyd and Coles, 2002; Lewis et al., 2004; Mcclure et al., 2004; Shohamy et al., 2004].”
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“While several functions have been associated with the striatum, the medial orbitofrontal cortex (mOFC) and the amygdala, it is widely accepted that they play a dominant role in processes related to reward anticipation and consumption, in the control of mood, and motivation, as well as in stimulus-response learning [14…”
BackgroundDisentangling motivational and experiential aspects of “utility” – A neuroeconomics perspective
Witt, U., & Binder, M. (2013) · Journal of Economic Psychology · doi:10.1016/j.joep.2013.02.001 · Cited by 15
“Learned reinforcers are always conditioned on primary reinforcers, even if the chain of associations may sometimes be quite long and idiosyncratic (see Cabanac, 1979; McClure et al., 2004).”
BackgroundInfluentialCovid-19 and Mental Health: Could Visual Art Exposure Help?
Gallo, L. M. H., Giampietro, V., Zunszain, P. A., & Tan, K. S. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.650314 · Cited by 19
From ensembles to meta-ensembles: Specific reward encoding by correlated network activity
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Problemas éticos en la investigación con neuromarketing: una revisión de la literatura
Lyu, D., & Mañas-Viniegra, L. (2021) · Vivat Academia · doi:10.15178/va.2021.154.e1351 · Cited by 14
“…científica que reafirma su importancia para identificar la estructura neuronal, así como ubicar la zona que puede influir la toma de decisiones (McClure et al, 2004; Deppe et al., 2007; Knutson et al., 2007; Hare et al., 2008; Grosenic et al., 2008; Santos et al, 2011; Levy & Glimcher, 2012;…”
BackgroundVentral Caudate and Anterior Insula Recruitment During Value Estimation of Passionate Rewarding Cues
Duarte, I. C., Coelho, G. F., Brito‐Costa, S., Cayolla, R. R., Afonso, S., & Castelo-Branco, M. S. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00678 · Cited by 13
“Incentive salience is a motivational property that may be elicited by reward-predicting cues (McClure et al., 2004; Berridge, 2012).”
BackgroundRodríguez-Gómez, P., Martín‐Loeches, M., Colmenares, F., Ferreiro, M. V. R., & Moreno, E. M. (2020) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-020-00773-w · Cited by 14
Remembering pleasure and personal meaning from episodes of intrinsic motivation: an fMRI study
Lee, W., & Reeve, J. (2020) · Motivation and Emotion · doi:10.1007/s11031-020-09855-1 · Cited by 13
Kanter, J. W., & Puspitasari, A. J. (2012) · Wiley eBooks · doi:10.1002/9781118470886.ch9 · Cited by 15
Neural correlates associated with conformity in adolescent and young adult men
Minich, M., Falk, E. B., Cooper, N., Cosme, D., Chan, H., Pei, R., O’Donnell, M. B., & Cascio, C. N. (2023) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2023.101215 · Cited by 20
“Alternatively, given the role of the VS and vmPFC in reward processing (McClure et al., 2004), it may be that late adolescents may be thinking more about the mental states of others and using that feedback to calculate expected reward of fitting in with others.”
BackgroundReward, Context, and Human Behaviour
Blaukopf, C. L., & DiGirolamo, G. J. (2007) · The Scientific World JOURNAL · doi:10.1100/tsw.2007.122 · Cited by 15
“The set of brain areas consistently activated in this work includes the striatum (caudate nucleus, putamen, and ventral striatum, including the nucleus accumbens), the amygdala, dopaminergic neural areas in the midbrain, and orbitofrontal cortex[4,5].”
BackgroundRodriguez‐Moreno, D. V., Cycowicz, Y. M., Figner, B., Wang, Z., He, X., Geronazzo‐Alman, L., Sun, X., Cheslack‐Postava, K., Bisaga, A. M., Hoven, C. W., et al. (2021) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2021.100942 · Cited by 12
“While some authors have suggested that the specific substance of abuse by parents is less important than the common risk factor among those who are FH+ (Tsuang et al., 1998), others have argued that familial risk for SUD is substance specific (Merikangas et al., 2009).”
BackgroundCorrelates of reward‐predictive value in learning‐related hippocampal neural activity
Okatan, M. (2009) · Hippocampus · doi:10.1002/hipo.20535 · Cited by 14
“…higher-order learning in humans, in the activity of brain areas involved in reward processing, including the ventral tegmental area, substantia nigra, and ventral striatum (McClure et al., 2003, 2004; O’Doherty et al., 2003; Montague et al., 2004, 2006; Seymour et al., 2004; Tanaka et al., 2004).”
Xiao, Y., Alkire, D. R., Moraczewski, D., & Redcay, E. (2022) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2022.101079 · Cited by 14
“These processes are supported by a reward network, including the orbitofrontal cortex (OFC), vmPFC, anterior cingulate cortex (ACC), bilateral ventral striatum (VS), and bilateral amygdala (Knutson et al., 2001; McClure et al., 2004; for a review, see Haber and Knutson, 2010).”
Paiva, G. C. D. C., Costa, D. D. S., Malloy‐Diniz, L. F., de Miranda, D. M., & de Paula, J. J. (2019) · Developmental Neuropsychology · doi:10.1080/87565641.2019.1667996 · Cited by 16
“However, McClure, York, and Montague (2004) emphasizes that rewardrelated aspects, such as type (primary or secondary rewards) and different magnitudes and delays, are directly related to the specific brain response.”
BackgroundInfluentialTrait Impulsivity and Choice Impulsivity in Young Adult Students With Probable Binge Eating Disorder
Zheng, D.-H., Liu, M., & Yan, W.-S. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.838700 · Cited by 15
Reward processing in the human brain
Porcelli, A. J., & Delgado, M. R. (2009) · Elsevier eBooks · doi:10.1016/b978-0-12-374620-7.00007-8 · Cited by 15
Neural basis of affect and emotion
Kirkland, T., & Cunningham, W. A. (2011) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.145 · Cited by 13
The Neurobiology of Emotion Regulation
Sebastian, C. L., & Ahmed, S. P. (2018) · Wiley eBooks · doi:10.1002/9781118650868.ch6 · Cited by 14
Neurobiological foundations and clinical relevance of effort-based decision-making
Brassard, S. L., Liu, H., Dosanjh, J., MacKillop, J. M., & Balodis, I. M. (2024) · Brain Imaging and Behavior · doi:10.1007/s11682-024-00890-x · Cited by 14
“Beyond EBDM paradigms, studies using the MIDT in healthy participants demonstrate distinct anticipation and outcome processes with reward anticipation linked to VS activation, and reward receipt linked to vmPFC activation Breiter et al., 2001; Knutson et al., 2000, 2001, 2003; McClure et al., 2004.”
Freitas, L. G. A., Liverani, M. C., Siffredi, V., Schnider, A., Tolsa, C. B., Leuchter, R. H., Ville, D. V. D., & Hüppi, P. S. (2021) · NeuroImage Clinical · doi:10.1016/j.nicl.2021.102668 · Cited by 9
“…and adaptive behaviors, such as executive abilities including assignment of value to a specific stimulus (Montague and Berns, 2002), prediction of specific outcomes (Rudebeck and Murray, 2014), reward processing (Kahnt, 2018), as well as decision making (Bechara, 2000; McClure et al., 2004).”
Cascio, C. N., Selkie, E. M., & Moreno, M. A. (2023) · JMIR Research Protocols · doi:10.2196/50984 · Cited by 11
“In both primary fMRI tasks (ie, self and other messages and Cyberball), the primary ROIs will be neural regions associated with social pain [108] and reward processing [114].”
BackgroundEffect of Number of Food Pieces on Food Selection and Consumption in Animals and Humans
Bajaj, D. (2013) · Cited by 9
O’Brien, J. W., Lichenstein, S. D., & Hill, S. Y. (2014) · Journal of Studies on Alcohol and Drugs · doi:10.15288/jsad.2014.75.643 · Cited by 10
Comorbidity implications in brain disease: Neuronal substrates of symptom profiles
Palomo, T., Beninger, R. J., Kostrzewa, R. M., & Archer, T. (2007) · Neurotoxicity Research · doi:10.1007/bf03033897 · Cited by 10
“…magnetic resonance imaging (fMRI), markedly superior to other neuroimaging techniques, provides direct estimates of neuronal activity, thereby information on neuronal substrates, pertaining to aspects of comorbid pathology in brain disorders (cf., Aber et al., 2003; McClure et al., 2004).”
BackgroundHassabElnaby, H. R., Abdel‐Maksoud, A., & Said, A. A. (2017) · Emerald Group Publishing Limited eBooks · doi:10.1108/s1475-148820170000020003 · Cited by 11
Why Losses Loom Larger than Gains: Modeling Neural Mechanisms of Cognitive-Affective Interaction
Eliasmith, C., Litt, A., & Thagard, P. R. (2006) · eScholarship (California Digital Library) · Cited by 10
Executive Compensation and Corporate Governance: Rising Above the “Pay‐for‐Performance” Principle
McConvill, J. A. (2006) · American Business Law Journal · doi:10.1111/j.1744-1714.2006.00021.x · Cited by 10
Electrophysiological Responses to Feedback during the Application of Abstract Rules
Walsh, M. M., & Anderson, J. R. (2013) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00454 · Cited by 11
Metadata
- Authors
- McClure, S. M., York, M. K., & Montague, P. R.
- Affiliations
- Baylor College of Medicine (US)
- Corresponding author
- McClure, Samuel M.
- Venue
- The Neuroscientist
- Publisher
- SAGE Publications
- Published
- 2004-06
- Volume
- 10
- Issue
- 3
- Pages
- 260-268
- ISSN
- 1073-8584 (ISSN-L)
- 1089-4098
- OpenAlex
- W2118755615
- Cited by
- 480
- References
- 63
- Citations by year
- 2026: 7 · 2025: 7 · 2024: 9 · 2023: 19 · 2022: 13 · 2021: 23 · 2020: 25 · 2019: 14 · 2018: 23 · 2017: 26 · 2016: 23 · 2015: 24 · 2014: 35 · 2013: 42 · 2012: 32
- FWCI
- 1.24
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Neuroscientist (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH052797)
- National Institute on Drug Abuse (R01DA011723)
- National Institute of Neurological Disorders and Stroke (K23NS041254)
- 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 › Clinical Psychology › Gambling Behavior and Treatments
- Keywords
- reward processing, neural correlates, ventral striatum, orbitofrontal cortex, amygdala, medial prefrontal cortex, reward timing, reward prediction, Parkinson's disease
- MeSH terms
- Algorithms, Animals, Brain, Humans, Magnetic Resonance Imaging, Neurons, Parkinson Disease, Radiography, Reward
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