The DOI matches its Crossref record; 62 of the 63 references it cites were found in a registry or an index.
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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BackgroundResultInfluentialHedonic and motivational roles of opioids in food reward: Implications for overeating disorders
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Embodied Brains, Social Minds, Cultural Meaning
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“A substantial body of literature has established that social feedback is encoded in similar parts of the valuation system as primary rewards such as food and sex (Bartra, McGuire, and Kable 2013; Lieberman and Eisenberger 2009; McClure, York, and Montague 2004).”
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“Incentivebased reasons for action are associated with neuronal responses in the (a) amygdala and striatum that process the rewarding properties of directly experienced environmental stimuli and (b) dorsolateral prefrontal cortex, orbitofrontal cortex, and cingulate cortex that process the learned reinforcement value o…”
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“Moreover, there is cognitive neuroscience evidence suggesting that the OFC region is involved in a network of rewardrelated regions (for review, see Martin-Soelch et al., 2001; McClure et al., 2004; O’Doherty, 2004; Rolls, 2000).”
BackgroundNeural correlates of a 'pessimistic' attitude when anticipating events of unknown emotional valence
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Unique brain areas associated with abstinence control are damaged in multiply detoxified alcoholics
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Neural evidence for Reference-dependence in real-market-transactions
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Like/dislike analysis using EEG: Determination of most discriminative channels and frequencies
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“These structures have been consistently implicated in the processing of positive feedback and monetary reward (McClure et al., 2004) and have previously been shown to be activated in a similar contrast (reward-punishment) in a probabilistic reversal task (Cohen et al., 2005).”
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“This general finding is consistent with previous fMRI studies associating the VS with reward prediction and anticipation of future reward and loss (Knutson et al. 2001; McClure et al. 2004; O’Doherty, 2004).”
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“Based on the role of these regions in reward processing [Carlson et al., 2011; Cromwell et al., 2005; McClure et al., 2004; Rushworth et al., 2011; Sescousse et al., 2015], our findings dovetail with the notion that downward comparison is experienced as rewarding [Bault et al., 2011; Dvash et al.,…”
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Neural correlates of reward and loss sensitivity in psychopathy
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“nately pleasurable stimuli, as well as to abstract stimuli predicting their occurrence (McClure et al., 2004; O’Doherty, 2004).”
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“…memory and uncertainty processing, and especially, the right part is associated with the perception of fair and unfair offers (Knoch et al., 2006; McClure et al., 2004; Sanfey et al., 2003; Schaefer et al., 2006) and plays a central role in linking the information about rewards to actual…”
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“This is consistent with previous fMRI studies associating these brain structures with reward prediction and choice of immediate reward (Diekhof and Gruber, 2010; Knutson et al, 2001; McClure et al, 2004; O’Doherty, 2004).”
Völlm, B., Richardson, P., McKie, S., Elliott, R., Dolan, M., & Deakin, B. (2007) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2007.04.008 · Cited by 92
“The role of the amygdala in reward processing has been proposed to be the detection of reward and salience (McClure et al., 2004).”
BackgroundInfluentialSelf-Regulation Without Force: Can Awareness Leverage Reward to Drive Behavior Change?
Ludwig, V. U., Brown, K. W., & Brewer, J. A. (2020) · Perspectives on Psychological Science · doi:10.1177/1745691620931460 · Cited by 85
van der Cruijsen, R., Peters, S., van der Aar, L. P. E., & Crone, E. A. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2017.11.005 · Cited by 78
Role of Frontostriatal Connectivity in Adolescents With Excessive Smartphone Use
Chun, J.-W., Choi, J.-Y., Cho, H., Choi, M.-R., Ahn, K., Choi, J.-S., & Kim, D. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00437 · Cited by 65
“Previous studies have identified the OFC and ventral striatum (VS), including the nucleus accumbens (NAcc), as a set of reward-related brain structures (22), Another imaging study reported that compared with healthy controls, chronic cocaine abusers had lower metabolism in the right OFC and NAcc, which was related to…”
BackgroundHormonal and Genetic Influences on Processing Reward and Social Information
Caldú, X., & Dreher, J. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1412.007 · Cited by 71
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Simulating social interactions for the experimental investigation of joint attention
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Intergroup social influence on emotion processing in the brain
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“The VS’s role in positive valuation and reward in previous studies (17, 19) might also suggest a difference in valuation occurring when viewing the feedback from ingroups and outgroups, and is consistent with previous evidence suggesting that the subjective value placed on stimuli is sensitive to social feedback (11,…”
ResultA comparison of the electrocortical response to monetary and social reward
Distefano, A., Jackson, F. L., Levinson, A. R., Infantolino, Z. P., Jarcho, J. M., & Nelson, B. D. (2018) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsy006 · Cited by 67
“It is plausible that the striatum is a key region involved in general reward processing and approachoriented behaviors (Delgado, 2007), while other brain regions are involved in higher-order processing of stimulus meaning and value (e.g. prefrontal cortex; McClure et al., 2004).”
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“Reward processing in health and illness Reward-directed behavior is fundamental to survival and well-being [1].”
BackgroundAltered processing of self-related emotional stimuli in mindfulness meditators
Lutz, J. G., Brühl, A. B., Doerig, N., Scheerer, H., Achermann, R. E., Weibel, A. A., Jäncke, L., & Herwig, U. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.09.057 · Cited by 62
“…evidence for increased emotional processing in LTM compared to MNP. LTM showed increased activation in the ventromedial orbitofrontal cortex/ventral striatum, which could indicate higher reward and subjective pleasantness of positive selfappraisals (Kühn and Gallinat, 2012; McClure et al., 2004).”
BackgroundAn imaging genetics approach to understanding social influence
Falk, E. B., Way, B. M., & Jasinska, A. J. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00168 · Cited by 62
“…to social norms include the ventral striatum (VS) and ventromedial prefrontal cortex (VMPFC), key structures in detecting salient inputs, and also key components of the brain’s reward system (Knutson et al., 2001; McClure et al., 2004b; Knutson and Cooper, 2005; Haber and Knutson, 2010).”
BackgroundBinge-eating disorder: Clinical and therapeutic advances
Hutson, P. H., Balodis, I. M., & Potenza, M. N. (2017) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2017.08.002 · Cited by 62
Neural correlates of 'pessimistic' attitude in depression
Herwig, U., Brühl, A. B., Kaffenberger, T., Baumgartner, T., Boeker, H., & Jäncke, L. (2010) · Psychological Medicine · doi:10.1017/s0033291709991073 · Cited by 56
“2007b) and thus not fulfilling the criteria for the ‘pessimism’contrast but being more generally associated with valence-independent emotional arousal (Anderson et al. 2003; McClure et al. 2004).”
BackgroundInfluentialNeural Correlates of Impulsive Buying Tendencies during Perception of Product Packaging
Hubert, M., Hubert, M., Florack, A., Linzmajer, M., & Kenning, P. (2013) · Psychology and Marketing · doi:10.1002/mar.20651 · Cited by 64
Acute Nicotine Differentially Impacts Anticipatory Valence- and Magnitude-Related Striatal Activity
Rose, E. J., Ross, T. J., Salmeron, B. J., Lee, M., Shakleya, D. M., Huestis, M. A., & Stein, E. A. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.06.034 · Cited by 59
Informing others is associated with behavioral and neural signatures of value.
Tamir, D., Zaki, J., & Mitchell, J. P. (2015) · Journal of Experimental Psychology General · doi:10.1037/xge0000122 · Cited by 59
Getting the word out: neural correlates of enthusiastic message propagation
Falk, E. B., O’Donnell, M. B., & Lieberman, M. D. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00313 · Cited by 58
“The VMPFC and VS are regions commonly associated with encoding reward and value signals (Knutson et al., 2001; McClure et al., 2004; Knutson and Cooper, 2005; Haber and Knutson, 2010).”
BackgroundPornpattananangkul, N., & Nusslock, R. (2016) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2016.07.037 · Cited by 58
“The main difference between Gray’s BAS reward-sensitivity and reward-processing used in the current study is that Gray did not separate BAS into temporal reward-processing stages as is common in contemporary neuroscientific theories (Berridge, 1996; McClure et al., 2004; Schultz et al., 2000; Wise, 2008).”
BackgroundMethodStallen, M., & Sanfey, A. G. (2013) · The Neuroscientist · doi:10.1177/1073858412469728 · Cited by 57
“So, to develop policy principles that can accurately predict the development, and ideally, the enhancement of cooperation, the formal models require elaboration with detailed information regarding the psychological principles that guide decisions in social interactions.”
BackgroundKorponay, C. H., Pujara, M. S., Deming, P., Philippi, C. L., Jean Decety, A., Kosson, D. S., Kiehl, K. A., & Koenigs, M. R. (2016) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2016.07.004 · Cited by 52
Abnormalities of functional brain networks in pathological gambling: a graph-theoretical approach
Tschernegg, M., Crone, J. S., Eigenberger, T., Schwartenbeck, P., Fauth‐Bühler, M., Leménager, T., Mann, K. F., Thon, N., Wurst, F. M., & Kronbichler, M. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00625 · Cited by 50
“The SMA is associated with motor execution and vigilance performance (Hinds et al., 2013) but is also involved in error detection and reward expectancy (McClure et al., 2004).”
BackgroundReward processing as a common diathesis for chronic pain and depression
Rizvi, S. J., Gandhi, W., & Salomons, T. V. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.04.033 · Cited by 50
Kamarajan, C., Rangaswamy, M., Manz, N., Chorlian, D. B., Pandey, A. K., Roopesh, B. N., & Porjesz, B. (2011) · Human Brain Mapping · doi:10.1002/hbm.21267 · Cited by 49
“…[e.g., Breiter and Rosen, 1999; Camara et al., 2008; Delgado et al., 2003, 2005; Knutson et al., 2000, 2001, 2003; MarcoPallares et al., 2007; McClure et al., 2004; Nieuwenhuis et al., 2005b], and a few imaging studies have documented the impairments in the key brain areas of reward…”
Transcranial direct current stimulation’s effect on novice versus experienced learning
Bullard, L., Browning, E. S., Clark, V., Coffman, B., García, C. M., Jung, R., Merwe, A., Paulson, K., Vakhtin, A., Wootton, C., et al. (2011) · Experimental Brain Research · doi:10.1007/s00221-011-2764-2 · Cited by 53
“It is also possible that if we are stimulating smaller regions within the PFC such as the orbitofrontal cortex, we could be facilitating emotional processing such as reward and decision making (McClure et al. 2004; Bechara et al. 2000), which is an important factor in our training paradigm.”
BackgroundConvergence of EEG and fMRI measures of reward anticipation
Gorka, S. M., Phan, K. L., & Shankman, S. A. (2015) · Biological Psychology · doi:10.1016/j.biopsycho.2015.09.007 · Cited by 45
“Second, both the ACC/mPFC and OFC are known to play major roles in emotion processing and are considered key components of the brain’s reward circuitry (Bush et al., 2000; McClure et al., 2004; Nestler & Carlezon, 2006).”
BackgroundNeural correlates of effective and ineffective mood induction
Kohn, N., Falkenberg, I., Kellermann, T., Eickhoff, S. B., Gur, R. C., & Habel, U. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst055 · Cited by 49
“We hypothesized that for effective MI, positive mood would be correlated with increased activation in the amygdala and the nucleus accumbens (NAcc) because of their involvement in reward processing (Cromwell and Schultz, 2003; McClure et al., 2004), placebo effects in pain (Scott et al.”
BackgroundBecker, A., Kirsch, M., Gerchen, M. F., Kiefer, F., & Kirsch, P. (2016) · Addiction Biology · doi:10.1111/adb.12352 · Cited by 45
“…evidence that the ventral striatum (VS), as a central node in the reward system, is activated by alcohol-associated cues and is thereby highly responsible for the incentive salience or ‘wanting’ for alcohol (Knutson & Cooper 2005; McClure et al. 2004; Robinson & Berridge 2001; Schacht et al. 2014).”
BackgroundAssociating resting-state connectivity with trait impulsivity
Angelides, N. H., Gupta, J., & Vickery, T. J. (2017) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsx031 · Cited by 48
“Ventral striatum (VS), including caudate nucleus and putamen, as well as subdivisions of orbitofrontal cortex (OFC), are often implicated in fMRI studies as involved in processing reward and impulsive behavior (O’Doherty et al., 2001; McClure et al., 2004, Kringelbach, 2005; Delgado, 2007).”
BackgroundInfluentialVerplaetse, J., Schrijver, J. D., Vanneste, S., & Braeckman, J. (2009) · Springer eBooks · doi:10.1007/978-1-4020-6287-2 · Cited by 49
Basal ganglia engagement during feedback processing after a substantial delay
Dobryakova, E., & Tricomi, E. M. (2013) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-013-0182-6 · Cited by 43
Brain mechanisms of social comparison and their influence on the reward system
Kedia, G., Mussweiler, T., & Linden, D. E. J. (2014) · Neuroreport · doi:10.1097/wnr.0000000000000255 · Cited by 46
“The VS reacts to both primary (e.g., pleasant tastes) and secondary rewards (e.g., monetary incentives) and seems to play a role in the formation of stimulus – reward association [22].”
BackgroundBrain Activation Associated with Pride and Shame
Roth, L., Kaffenberger, T., Herwig, U., & Brühl, A. B. (2014) · Neuropsychobiology · doi:10.1159/000358090 · Cited by 47
Bae, S., Han, D. H., Jung, J., Nam, K., & Renshaw, P. F. (2017) · Journal of Behavioral Addictions · doi:10.1556/2006.6.2017.061 · Cited by 43
“, 2010), and the left/right amygdala for the reward circuitry (Haber & Knutson, 2010; McClure et al., 2004; Schultz, 2006).”
BackgroundMethodCognitive impairment and fMRI in major depression
Ebmeier, K. P., Rose, E. J., & Steele, J. D. (2006) · Neurotoxicity Research · doi:10.1007/bf03033237 · Cited by 42
“As with reward learning in normal healthy adults (Berns et al., 2001; McClure et al., 2004), emotional learning in depression is associated with neural "predictive error" signals (Steele et al., 2004).”
BackgroundStepien, M., Manoliu, A., Kubli, R., Schneider, K., Tobler, P. N., Seifritz, E., Herdener, M., Kaiser, S., & Kirschner, M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0198215 · Cited by 45
Reduced cerebellar brain activity during reward processing in adolescent binge drinkers
Cservenka, A., Jones, S. A., & Nagel, B. J. (2015) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.06.004 · Cited by 41
“…such as the orbitofrontal cortex (OFC), medial prerontal cortex (mPFC), and striatum have been implicated as key omponents in the brain’s reward system (McClure et al., 2004; chultz, 2000) and are regions that undergo development durng adolescence (Goddings et al., 2014; Gogtay et al., 2004).”
Reward Sensitivity Is Associated with Brain Activity during Erotic Stimulus Processing
Costumero, V., Barrós-Loscertales, A., Bustamante, J. C., Ventura-Campos, N., Fuentes, P., Rosell-Negre, P., & Ávila, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066940 · Cited by 45
“This area has been implicated in coding the current value of stimuli [58–60], holding them in working memory to anticipate future consequences of behavior [42,57].”
BackgroundKoch, K., Wagner, G., Schachtzabel, C., Schultz, C. C., Güllmar, D., Reichenbach, J. R., Sauer, H., Zimmer, C., & Schlösser, R. G. M. (2014) · Human Brain Mapping · doi:10.1002/hbm.22284 · Cited by 42
“…orbital frontal cortex (OFC), medial prefrontal cortex (MPFC), amygdala, insula and the ventral striatum has been identified—all areas innervated by mesolimbic dopamine projections [Camara et al., 2009; Cauda et al., 2011; Knutson et al., 2003; McClure et al., 2004; Yacubian et al., 2006].”
BackgroundWhat shall I be, what must I be: neural correlates of personal goal activation
Strauman, T. J., Detloff, A. M., Sestokas, R., Smith, D. V., Davis, E., Rivera, C., & Kwapil, L. (2013) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2012.00123 · Cited by 40
“…striatum and ventromedial prefrontal cortex, with the former a locus for the coding of predictions regarding positive outcomes and the latter important for the processing of the hedonic significance of stimuli (Bjork et al., 2004; McClure et al., 2004; Kringelbach, 2005; Clithero et al., 2011).”
BackgroundCognitive Neuroscience Perspectives on Motivation and Learning: Revisiting Self‐Determination Theory
Luria, E., Shalom, M., & Levy, D. A. (2020) · Mind Brain and Education · doi:10.1111/mbe.12275 · Cited by 62
Dimoka, A. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.05.007 · Cited by 44
“These areas are also part of the brain's “reward” areas (McClure et al., 2004); specifically the caudate nucleus is associated by themagnitudeof a reward (Hsu et al.”
InfluentialCooper, J. C., Dunne, S., Furey, T., & O'Doherty, J. P. (2014) · Cerebral Cortex · doi:10.1093/cercor/bht102 · Cited by 39
“This is consistent with its role in representing experienced utility in a variety of non-social and social domains (Davey et al., 2009; McClure et al., 2004; O’Doherty et al., 2003; O’Doherty, 2004; Plassmann et al., 2007).”
Bases neurales de la toma de decisiones
Broche‐Pérez, Y., Jiménez, L. F. H., & Martínez, E. O. (2015) · Neurología · doi:10.1016/j.nrl.2015.03.001 · Cited by 51
Brain-Friendly Strategies for the Inclusion Classroom
Willis, J. (2007) · Cited by 38
How does cognitive reappraisal affect the response to gains and losses?
Yang, Q., Gu, R., Tang, P., & Luo, Y. (2013) · Psychophysiology · doi:10.1111/psyp.12091 · Cited by 40
Barrós‐Loscertales, A., Ventura‐Campos, N., Sanjuán, A., Belloch, V., Parcet, M. A., & Ávila, C. (2010) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsq012 · Cited by 43
“On the other hand, the OFC has been proposed to be an area for storing the reward value of sensory stimuli (McClure et al., 2004), while its function has been related to the processing of secondary emotional stimuli (Kawabata and Zeki, 2004; Meseguer et al., 2007), reward prediction (Critchley et…”
BackgroundResultInfluentialOpioid Modulation of Value-Based Decision-Making in Healthy Humans
Eikemo, M., Biele, G., Willoch, F., Thomsen, L., & Leknes, S. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.58 · Cited by 39
“Indeed, brain regions richly innervated by MORs such as ventral striatum, amygdala and perigenual anterior cingulate cortex have been consistently implicated in human neuroimaging studies of monetary and other rewards (McClure et al, 2004).”
Background
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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