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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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Conflict of Interest in Medical Research, Education, and Practice
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BackgroundWhy Don't We Move Faster? Parkinson's Disease, Movement Vigor, and Implicit Motivation
Mazzoni, P., Hristova, A., & Krakauer, J. W. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0264-07.2007 · Cited by 557
“Perhaps this is because PD primarily affects movement parameters, which are specified implicitly, whereas the traditional motivation framework developed for reward-guided behavior emphasizes explicit choices (Niv et al., 2006; Schultz, 2006) (but see McClure et al., 2004).”
BackgroundDisclosing information about the self is intrinsically rewarding
Tamir, D. I., & Mitchell, J. P. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202129109 · Cited by 563
Bickel, W. K., Miller, M. L., Yi, R., Kowal, B. P., Lindquist, D. M., & Pitcock, J. A. (2007) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2006.09.016 · Cited by 571
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“Neuroimaging experiments have extended these results to humans by demonstrating that blood-oxygen level-dependent (BOLD) responses in the striatum and prefrontal cortex, regions innervated by dopamine neurons, mirror reward prediction errors as well (McClure et al., 2004; O’Doherty, 2004).”
BackgroundWhen your gain is my pain and your pain is my gain: neural correlates of envy and schadenfreude
Takahashi, H., Kato, M., Matsuura, M., Mobbs, D., Suhara, T., & Okubo, Y. (2009) · Science · doi:10.1126/science.1165604 · Cited by 508
An automatic valuation system in the human brain: Evidence from functional neuroimaging
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“Interestingly, regions comprising the limbic frontostriatal circuits have been implicated in both valuation and choice tasks (Hare et al., 2009; Kim et al., 2007; Knutson et al., 2007; McClure et al., 2004b; Paulus and Frank, 2003; Plassmann et al., 2008).”
InfluentialCarlson, J. M., Foti, D., Mujica-Parodi, L. R., Harmon‐Jones, E., & Hajcak, G. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.05.037 · Cited by 490
“…latter finding is noteworthy in light of neuroimaging evidence that, like modulation of the FN, striatal activation is sensitive to outcome valence, but not magnitude (Elliott et al., 2003), and that it is sensitive to violations of reward predictions (McClure et al., 2004; O'Doherty et al., 2003).”
BackgroundDisentangling pleasure from incentive salience and learning signals in brain reward circuitry
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Lack of Ventral Striatal Response to Positive Stimuli in Depressed Versus Normal Subjects
Epstein, J., Pan, H., Kocsis, J. H., Yang, Y., Butler, T., Chusid, J., Hochberg, H., Murrough, J., Strohmayer, E., Stern, E., et al. (2006) · American Journal of Psychiatry · doi:10.1176/ajp.2006.163.10.1784 · Cited by 464
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Foti, D., Weinberg, A., Dien, J., & Hajcak, G. (2011) · Human Brain Mapping · doi:10.1002/hbm.21182 · Cited by 467
“The processing of rewards involves a network of brain regions that includes not only the striatum but also the amygdala, medial prefrontal cortex, and orbitofrontal cortex [McClure et al., 2004], each of which may contribute to scalp-recorded EEG activity.”
BackgroundA multifaceted investigation of the link between mental fatigue and task disengagement
Hopstaken, J. F., van der Linden, D., Bakker, A. B., & Kompier, M. A. J. (2014) · Psychophysiology · doi:10.1111/psyp.12339 · Cited by 503
Prediction error in reinforcement learning: A meta-analysis of neuroimaging studies
Garrison, J. R., Erdeniz, B., & Done, J. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.023 · Cited by 460
Gender difference in neural response to psychological stress
Wang, J., Korczykowski, M., Rao, H., Yong Fan, A., Pluta, J. B., Gur, R. C., McEwen, B. S., & Detre, J. A. (2007) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsm018 · Cited by 447
“Within this theoretical framework, the observed ventral striatum activation might indicate an intrinsic neurobiological mechanism of the female brain to activate the reward system under stress, thereby down-regulating the ‘fight-or-flight’ response.”
BackgroundOldham, S., Murawski, C., Fornito, A., Youssef, G. J., Yücel, M., & Lorenzetti, V. (2018) · Human Brain Mapping · doi:10.1002/hbm.24184 · Cited by 449
“Such a signal would be critical for reward processing and learning, increasing the likelihood a behaviour that leads to a better than expected outcome will be repeated (McClure et al., 2004; Schultz &Dickinson, 2007; Yacubian et al., 2006), like in the MIDT.”
BackgroundSimilar neural responses predict friendship
Parkinson, C., Kleinbaum, A. M., & Wheatley, T. (2018) · Nature Communications · doi:10.1038/s41467-017-02722-7 · Cited by 388
Schönberg, T., Daw, N. D., Joel, D., & O'Doherty, J. P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2496-07.2007 · Cited by 390
Immaturities in reward processing and its influence on inhibitory control in adolescence.
Geier, C. F., Terwilliger, R., Teslovich, T., Velanova, K., & Luna, B. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp225 · Cited by 396
“In particular, the orbitofrontal cortex (OFC), dorsal and ventral striatum (VS), and medial prefrontal cortex (PFC) have been identified as key compo- nents (Schultz 2000; McClure et al. 2004).”
BackgroundInfluentialPrelude to Passion: Limbic Activation by “Unseen” Drug and Sexual Cues
Childress, A. R., Ehrman, R. N., Wang, Z., Li, Y., Sciortino, N., Hakun, J. G., Jens, W., Suh, J. J., Listerud, J., Marquez, K., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001506 · Cited by 395
“We used the large number of prior published articles describing the interconnected circuitry activated by reward cues [12] (see supplemental Anatomical Comments in Text S1) to limit our hypotheses and interpretations to regions of strong a priori interest.”
BackgroundMethodBasal ganglia orient eyes to reward
Hikosaka, O., Nakamura, K., & Nakahara, H. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00458.2005 · Cited by 377
Why gamblers fail to win: A review of cognitive and neuroimaging findings in pathological gambling
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Effort discounting in human nucleus accumbens
Botvinick, M., Huffstetler, S., & McGuire, J. T. (2009) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.9.1.16 · Cited by 364
“Nevertheless, the ability to perform cost– benefit analyses depends on knowledge gleaned from previous experience with reward (McClure et al., 2004; O’Doherty et al., 2003) and effort (Botvinick, 2007) outcomes.”
BackgroundResultInfluentialRao, H., Korczykowski, M., Pluta, J. B., Hoang, A., & Detre, J. A. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.05.046 · Cited by 366
“Based on the critical role of dopamine rich mesolimbic structures in both reward and emotion processing (Bozarth, 1991; Delgado, 2007;Schultz 2007) aswell as the consistent activation in these regions associatedwith risk and reward (McClure et al., 2004; Hsu et al., 2005; Montague et al., 2006; Preuschoff et al., 2006…”
BackgroundDissociation of neural networks for anticipation and consumption of monetary and social rewards
Rademacher, L., Krach, S., Kohls, G., Irmak, A., Gründer, G., & Spreckelmeyer, K. N. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.10.089 · Cited by 347
“…(NAcc)), amygdala, orbital frontal and mesial prefrontal cortex, function as the reward system of the brain, attributing a special role to dopamine as the innervating neurotransmitter (see (Arias-Carrion and Poppel, 2007; McClure et al., 2004; O'Doherty, 2004; Schultz, 2006) for reviews).”
A current overview of consumer neuroscience
Hubert, M., & Kenning, P. H. (2008) · Journal of Consumer Behaviour · doi:10.1002/cb.251 · Cited by 390
“Jour on learned expectations, context, time dimensions, and reward amplitude (McClure et al., 2004b).”
BackgroundMethodResultInfluentialDiekhof, E. K., Kaps, L., Falkai, P., & Gruber, O. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.02.007 · Cited by 332
Subliminal Instrumental Conditioning Demonstrated in the Human Brain
Pessiglione, M., Petrovic, P., Daunizeau, J., Palminteri, S., Dolan, R. J., & Frith, C. D. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.005 · Cited by 308
“Computational Model We used a standard Q-learning algorithm (Sutton and Barto, 1998), which has been shown previously to offer a good account of instrumental choice in both humans and monkeys (Daw and Doya, 2006; McClure et al., 2004; O’Doherty et al., 2007).”
BackgroundMethodNeural mechanisms underlying motivation of mental versus physical effort
Schmidt, L., Lebreton, M., Cléry-Melin, M.-L., Daunizeau, J., & Pessiglione, M. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001266 · Cited by 310
“The so-called brain valuation system (BVS), which was shown to express preferences, pleasantness ratings, and reward expectations [12–17], mainly includes the ventral prefrontal cortex and its basal ganglia (BG) target, the ventral striatum.”
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Neurobiological mechanisms of anhedonia
Gorwood, P. (2008) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2008.10.3/pgorwood · Cited by 285
“The ventral striatum, and particularly the nucleus accumbens,(40) may indeed have a priority role according to studies in both animals and humans, in behavioral responses to, anticipation of, and/or monitoring of errors in the prediction of reward.(41,42) The nucleus accumbens appears to respond to the emotional inten…”
NeuroEconomics: An overview from an economic perspective
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Silverman, M. H., Jedd, K., & Luciana, M. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.07.083 · Cited by 277
“Accordingly, 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).”
O'Hara, C., Campbell, I. C., & Schmidt, U. H. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.02.012 · Cited by 271
Neural representation of reward in recovered depressed patients
McCabe, C., Cowen, P. J., & Harmer, C. J. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1573-9 · Cited by 248
“For example, McClure et al. (2004) proposed that impaired activity in the ventral striatum to reward could be associated with a lessened ability to learn stimulus–reward associations resulting in a failure to bias goal-directed behavior appropriately.”
BackgroundReward-Dependent Modulation of Neuronal Activity in the Primate Dorsal Raphe Nucleus
Nakamura, K., Matsumoto, M., & Hikosaka, O. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0021-08.2008 · Cited by 246
“Recent studies have suggested that multiple neural systems may participate in the representation of rewards at different timescales (McClure et al., 2004; Tanaka et al., 2004).”
BackgroundDimoka, A., Pavlou, P. A., & Davis, F. D. (2010) · Information Systems Research · doi:10.1287/isre.1100.0284 · Cited by 253
“2001), and timing of rewards (McClure et al. 2004a) to devise appropriate compensation schemes for IT professionals.”
BackgroundInfluentialNeural systems underlying approach and avoidance in anxiety disorders
Robin L., A., & Martin, P. P. (2010) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2010.12.4/raupperle · Cited by 227
The Nucleus Accumbens and Pavlovian Reward Learning
Day, J. J., & Carelli, R. M. (2007) · The Neuroscientist · doi:10.1177/1073858406295854 · Cited by 235
Increased neural processing of rewarding and aversive food stimuli in recovered anorexia nervosa
Cowdrey, F. A., Park, R. J., Harmer, C. J., & McCabe, C. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.028 · Cited by 233
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The maturation of incentive processing and cognitive control
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“Neuroimaging studies in humans have identified similar regions in adults (Thut et al., 1997; O’Doherty, 2004; McClure et al., 2004; Delgado et al., 2000; Knutson et al., 2000; Breiter et al., 2001; Delgado et al., 2003; Elliott et al., 2003).”
BackgroundJarbo, K., & Verstynen, T. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2636-14.2015 · Cited by 228
Alcohol, psychological dysregulation, and adolescent brain development
Clark, D. B., Thatcher, D. L., & Tapert, S. F. (2008) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.2007.00601.x · Cited by 222
Genetic origins of social networks in rhesus macaques
Brent, L. J. N., Heilbronner, S. R., Horvath, J. E., Gonzalez-Martinez, J., Ruiz-Lambides, A., Robinson, A. G., Skene, J. H. P., & Platt, M. L. (2013) · Scientific Reports · doi:10.1038/srep01042 · Cited by 220
Monetary Reward Processing in Obese Individuals With and Without Binge Eating Disorder
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“…for the inconsistency with the present study and evidence linking medial OFC to processing moral goodness (Moll et al., 2006; Zahn et al., 2008) and rewarding stimuli (Rolls, 2000; Martin-Soelch et al., 2001; McClure et al., 2004; O'Doherty, 2004) are uncertain and deserve further research.”
InfluentialPadmanabhan, A., Geier, C. F., Ordaz, S. J., Teslovich, T., & Luna, B. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.06.004 · Cited by 202
“, 1992) and may underlie bias for immediate over future rewards (McClure et al., 2004).”
Kang, M. J., Hsu, M., Krajbich, I. M., Loewenstein, G. F., McClure, S. M., Wang, J. T., & Camerer, C. (2008) · SSRN Electronic Journal · doi:10.2139/ssrn.1308286 · Cited by 214
Self-citationOp de Macks, Z. A., Moor, B. G., Overgaauw, S., Güroğlu, B., Dahl, R. E., & Crone, E. A. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.06.003 · Cited by 203
“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).”
Feld, L. P., & Frey, B. S. (2006) · SSRN Electronic Journal · doi:10.2139/ssrn.900366 · Cited by 201
Modulation of the brain activity in outcome evaluation by interpersonal relationship: An ERP study
Leng, Y., & Zhou, X. (2009) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2009.10.002 · Cited by 201
A dual‐systems perspective on addiction: contributions from neuroimaging and cognitive training
McClure, S. M., & Bickel, W. K. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12561 · Cited by 209
Self-citationAmotivation in Schizophrenia: Integrated Assessment With Behavioral, Clinical, and Imaging Measures
Wolf, D. H., Satterthwaite, T. D., Kantrowitz, J. J., Katchmar, N., Vandekar, L., Elliott, M. A., & Ruparel, K. (2014) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu026 · Cited by 216
Novak, K. D., & Foti, D. (2015) · Psychophysiology · doi:10.1111/psyp.12504 · Cited by 205
Nicotine Dependence Is Characterized by Disordered Reward Processing in a Network Driving Motivation
Bühler, M., Vollstädt-Klein, S., Kobiella, A., Budde, H., Reed, L. J., Braus, D. F., Büchel, C., & Smolka, M. N. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.10.029 · Cited by 185
“e focus our report on the mesocorticolimbic system including he anterior cingulate cortex (Brodmann’s area 24, 25, 32, and 3), orbitofrontal and medial prefrontal regions, globus pallidus, audate nucleus, and putamen comprising the ventral striatum nd the ventral tegmental area because this brain network is ritically…”
BackgroundSelf-related awareness and emotion regulation
Herwig, U., Kaffenberger, T., Jäncke, L., & Brühl, A. B. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.12.089 · Cited by 189
“In parallel, amygdalar activation as an indicator for emotional arousal (McClure et al., 2004) was diminished during affect labeling of external cues with increasing mindfulness (Creswell et al.”
The importance of context: When relative relief renders pain pleasant
Leknes, S., Berna, C., Lee, M., Snyder, G. D., Biele, G., & Tracey, I. (2012) · Pain · doi:10.1016/j.pain.2012.11.018 · Cited by 187
“Moreover, relative to the control stimulus, moderate pain in the relative relief context showed higher activation in vmPFC regions, consistent with the increased hedonic value of this stimulus [29,40,43,46,51,61].”
BackgroundCosta Dias, T. G., Wilson, V. B., Bathula, D. R., Iyer, S. P., Mills, K. L., Thurlow, B. L., Stevens, C. A., Musser, E. D., Carpenter, S. D., Grayson, D. S., et al. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2012.10.015 · Cited by 180
“These findings are consistent with the hypothesis that atypical signaling of the NAcc to the prefrontal cortex in ADHD may lead to excessive approach and failure in estimating future consequences; thus, leading to impulsive behavior.”
BackgroundResultInfluentialBrain correlates of aesthetic expertise: A parametric fMRI study
Kirk, U., Skov, M., Christensen, M. S., & Nygaard, N. (2009) · Brain and Cognition · doi:10.1016/j.bandc.2008.08.004 · Cited by 224
Richards, J. M., Plate, R. C., & Ernst, M. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.004 · Cited by 174
“This neural system comprises subcortical and cortical structures that are major sites of dopamine action, and include primarily the striatum (caudate nucleus, putamen and nucleus accumbens) (e.g., Di Chiara, 2002; Di Chiara and Bassareo, 2007; McClure et al., 2004; Schultz et al., 1998; Wise, 2004) and the medial and…”
BackgroundRole of Dopamine in the Primate Caudate Nucleus in Reward Modulation of Saccades
Nakamura, K., & Hikosaka, O. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4853-05.2006 · Cited by 179
Altered neural reward and loss processing and prediction error signalling in depression
Ubl, B., Kuehner, C., Kirsch, P., Ruttorf, M., Diener, C., & Flor, H. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsu158 · Cited by 165
“Our results furthermore point to a reduced ability to learn stimulus-reward associations, possibly leading to significant alterations in approach behaviour in depression (McClure et al., 2004; den Ouden et al., 2012).”
ResultNeural reward processing is modulated by approach- and avoidance-related personality traits
Simon, J. J., Walther, S., Fiebach, C. J., Friederich, H.-C., Stippich, C., Weisbrod, M., & Kaiser, S. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.09.016 · Cited by 174
“On the other hand, the ventral striatum (VS) is considered a primary locus for the coding of the prediction error, which is important for learning stimulus-reward associations and action selection for the obtainment of rewards (McClure et al., 2004; Schultz et al., 1997).”
BackgroundGABAergic output of the basal ganglia
Hikosaka, O. (2007) · Progress in brain research · doi:10.1016/s0079-6123(06)60012-5 · Cited by 171
“…cortex is modulated by expected reward in monkeys (Watanabe, 1996; Platt and Glimcher, 1999; Tremblay and Schultz, 2000; Kobayashi et al., 2002; Roesch and Olson, 2003; Sugrue et al., 2004; Amiez et al., 2006) and in humans (O'Doherty et al., 2001; Ramnani and Miall, 2003; McClure et al., 2004).”
BackgroundIto, R., & Lee, A. C. H. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.07.039 · Cited by 188
Modulation of anticipatory emotion and perception processing by cognitive control
Herwig, U., Baumgärtner, T., Kaffenberger, T., Brühl, A. B., Kottlow, M., Schreiter-Gasser, U., Abler, B., Jäncke, L., & Rufer, M. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.05.023 · Cited by 170
“, 2001), but also with pleasant emotional stimuli (Canli et al., 2002; Garavan et al., 2001; Hamann and Mao, 2002; McClure et al., 2004), reward-related processing (Breiter and Rosen, 1999; Gottfried et al.”
BackgroundResultInfluentialREMIJNSE, P., NIELEN, M., UYLINGS, H., & VELTMAN, D. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.02.009 · Cited by 163
Individual differences in reward–prediction–error: extraversion and feedback-related negativity
Smillie, L. D., Cooper, A. J., & Pickering, A. D. (2010) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsq078 · Cited by 170
“The observation that rewards alter behaviour is now widely explained in terms of the mesencephalic dopamine (DA) system and its role in behavioural adaptation (Robbins and Everitt, 1996; McClure et al., 2004; Schultz, 2007).”
BackgroundNeural mechanisms of social decision-making in the primate amygdala
Chang, S. W. C., Fagan, N. A., Toda, K., Utevsky, A. V., Pearson, J. M., & Platt, M. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514761112 · Cited by 157
“One possibility is that ACCg may compute signals relevant for assigning credit or agency to the recipients of rewards (50) or shared experience (51, 52), whereas the amygdala may compute reward prediction or outcome signals relevant for making decisions (53, 54) or learning (18, 55).”
Pfabigan, D. M., Seidel, E., Sladky, R., Hahn, A., Paul, K., Grahl, A., Küblböck, M., Kraus, C., Hummer, A., Kranz, G. S., et al. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.03.077 · Cited by 166
“…ventral striatum including nucleus accumbens (NAcc), amygdala , and orbital mesial parts of the prefrontal cortex are chiefly involved in reward processing (e.g., Arias-Carrion and Poppel, 2007; Liu et al., 2011; McClure et al., 2004; O'Doherty, 2004; Schultz, 2006; Sescousse et al., 2013).”
Distorted expectancy coding in problem gambling: is the addictive in the anticipation?
van Holst, R. J., Veltman, D. J., Büchel, C., van den Brink, W., & Goudriaan, A. E. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.12.030 · Cited by 155
Smillie, L. D., Cooper, A. J., Wilt, J. A., & Revelle, W. (2012) · Journal of Personality and Social Psychology · doi:10.1037/a0028372 · Cited by 167
Striatal sensitivity to reward deliveries and omissions in substance dependent patients
Bjork, J. M., Smith, A. R., & Hommer, D. W. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.06.035 · Cited by 154
Satterthwaite, T. D., Green, L., Myerson, J., Parker, J. B., Ramaratnam, M., & Buckner, R. L. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.04.066 · Cited by 160
“These imaging studies have consistently observed reward-related activity in the striatum (for reviews, see Knutson and Cooper, 2005; McClure et al., 2004), which are known to receive significant DA projections from the midbrain (Lidow et al.”
BackgroundPower, Y., Goodyear, B. G., & Crockford, D. N. (2011) · Journal of Gambling Studies · doi:10.1007/s10899-011-9278-5 · Cited by 147
“Studies using monetary rewards generally suggest that abnormalities in orbitofrontal (OFC) and ventromedial prefrontal cortex (vmPFC), as well as striatal regions, may be present in PG subjects (McClure et al. 2004; Potenza 2008).”
BackgroundNeuroimaging for drug addiction and related behaviors
Parvaz, M. A., Alia-Klein, N., Woicik, P. A., Volkow, N. D., & Goldstein, R. Z. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.055 · Cited by 151
“…function in dopaminergically innervated corticolimbic areas [encompassing the orbitofrontal cortex (OFC) and anterior cingulate cortex (ACC)] that mediate processing of reward salience, motivation, and inhibitory control (Volkow et al. , 1993a ; McClure et al. , 2004 ; Goldstein et al. , 2007a ).”
Heide, R. J. V. D., Vyas, G., & Olson, I. R. (2014) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsu009 · Cited by 148
“This suggests that bilateral amygdala activations might actually relate to how arousing or salient the stimuli are to individuals viewing them (McClure et al., 2004).”
BackgroundFunctional connectivity of reward processing in the brain
Camara, E. (2008) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.019.2008 · Cited by 141
“This pattern agrees with previous fMRI studies that underscored the fundamental role of this neural network in the encoding, updating, and maintenance of rewards and punishments (Breiter et al., 2001; Delgado et al., 2000, 2003; Knutson et al., 2001, 2003; McClure et al., 2004; Riba et al., 2008; Tom et al., 2007; Yac…”
BackgroundResultMotivating forces of human actions
Walter, H., Abler, B., Ciaramidaro, A., & Erk, S. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.06.016 · Cited by 149
Rutherford, H. J. V., Williams, S. K., Moy, S., Mayes, L. C., & Johns, J. M. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00037 · Cited by 140
“Widespread use of fMRI has also enabled reward circuitry in humans to be investigated, with comparable regions identified, including the orbitofrontal cortex (OFC), amygdala, NAc, as well as the PFC and anterior cingulate cortex (ACC; McClure et al., 2004).”
BackgroundRevisiting the Role of Rewards in Motivation and Learning: Implications of Neuroscientific Research
Hidi, S. E. (2015) · Educational Psychology Review · doi:10.1007/s10648-015-9307-5 · Cited by 167
Neural response to reward anticipation is modulated by Gray's impulsivity
Hahn, T., Dresler, T., Ehlis, A.-C., Plichta, M. M., Heinzel, S., Polak, T., Lesch, K.-P., Breuer, F., Jakob, P. M., & Fallgatter, A. J. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.03.038 · Cited by 136
“In summary, the VS, the amygdala and the OFC have been consistently implicated in reward processing (McClure et al., 2004).”
Striatum gray matter reduction in males with an overactive behavioral activation system
Barrós‐Loscertales, A., Meseguer, V., Sanjuán, A., Belloch, V., Parcet, M. A., Torrúbia, R., & Ávila, C. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05084.x · Cited by 138
“Reward is processed in the brain using a network that includes the orbitofrontal system, medial prefrontal cortex, striatum and amygdala (McClure et al., 2004).”
BackgroundTsukiura, T., & Cabeza, R. E. L. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.07.046 · Cited by 139
“The sensitivity of OFC to socially positive facial stimuli could reflect the important role of this region in processing reward signals (Martin- Soelch et al., 2001; McClure et al., 2004; O'Doherty, 2004; Rolls, 2000).”
Influentialde Guinea, A. O., Titah, R., & Léger, P. (2014) · Journal of Management Information Systems · doi:10.2753/mis0742-1222300407 · Cited by 132
“the caudate nucleus and anterior cingulated cortex are activated by large rewards [60, 75] and the anticipation of rewards [40], respectively.”
BackgroundGet Aroused and Be Stronger: Emotional Facilitation of Physical Effort in the Human Brain
Schmidt, L., Cléry-Melin, M.-L., Lafargue, G., Valabrègue, R., Fossati, P., Dubois, B., & Pessiglione, M. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1951-09.2009 · Cited by 123
“Consistently, it has been regularly associated with reward anticipation or receipt in functional neuroimaging studies (McClure et al., 2004; Knutson and Cooper, 2005; Peciña et al., 2006).”
BackgroundSmillie, L. D. (2008) · European Journal of Personality · doi:10.1002/per.674 · Cited by 133
“In the case of the reward system or BAS, neuroimaging studies in humans have confirmed results of animal data concerning the role of the DA-innervated brain regions in reward processing (e.g. Knutson & Cooper, 2005; McClure et al., 2004).”
ResultMoore, W. E., Pfeifer, J. H., Masten, C. L., Mazziotta, J. C., Iacoboni, M., & Dapretto, M. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsr066 · Cited by 115
Reward networks in the brain as captured by connectivity measures
Càmara, E. (2009) · Frontiers in Neuroscience · doi:10.3389/neuro.01.034.2009 · Cited by 120
“Choices of immediately available rewards are mediated by the activity of limbic regions, while choices of long-term rewards are supported by the activity of prefrontal regions (McClure et al., 2004).”
InfluentialAbler, B., Erk, S., & Walter, H. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0690-y · Cited by 118
“Neuroimaging studies in humans confirmed the involvement of dopaminergic brain regions in reward processes (reviews in: Knutson and Cooper 2005; McClure et al. 2004).”
BackgroundNeuroeconomic Studies of Impulsivity: Now or Just as Soon as Possible?
Glimcher, P. W., Kable, J. W., & Louie, K. (2007) · American Economic Review · doi:10.1257/aer.97.2.142 · Cited by 118
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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