Reward processing in primate orbitofrontal cortex and basal ganglia
Abstract
This article reviews and interprets neuronal activities related to the expectation and delivery of reward in the primate orbitofrontal cortex, in comparison with slowly discharging neurons in the striatum (caudate, putamen and ventral striatum, including nucleus accumbens) and midbrain dopamine neurons. Orbitofrontal neurons showed three principal forms of reward-related activity during the performance of delayed response tasks, namely responses to reward-predicting instructions, activations during the expectation period immediately preceding reward and responses following reward. These activations discriminated between different rewards, often on the basis of the animals' preferences. Neurons in the striatum were also activated in relation to the expectation and detection of reward but in addition showed activities related to the preparation, initiation and execution of movements which reflected the expected reward. Dopamine neurons responded to rewards and reward-predicting stimuli, and coded an error in the prediction of reward. Thus, the investigated cortical and basal ganglia structures showed multiple, heterogeneous, partly simultaneous activations which were related to specific aspects of rewards. These activations may represent the neuronal substrates of rewards during learning and established behavioral performance. The processing of reward expectations suggests an access to central representations of rewards which may be used for the neuronal control of goaldirected behavior.
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Phasic bursts are large when an organism encounters novel rewarding stimuli or when cues during learning indicate the possibility of a valued reward when reward delivery is uncertain.
“Phasic bursts are large when an organism encounters novel rewarding stimuli (Schultz et al., 2000) or when cues during learning indicate the possibility of a valued reward when reward delivery is uncertain.”
From Incentive Motivation, Cognitive Control, and the Adolescent Brain: Is It Time for a Paradigm Shift? (2012) · cites this paper as Schultz et al., 2000
When reward delivery is fully predictable from experience, phasic firing declines, indicating that learning is established.
“When reward delivery is fully predictable from experience, phasic firing declines, indicating that learning is established (Schultz et al., 2000).”
From Incentive Motivation, Cognitive Control, and the Adolescent Brain: Is It Time for a Paradigm Shift? (2012) · cites this paper as Schultz et al., 2000
Cites
A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · see citing works
Self-citationRescorla, R. A. (1972) · Medical Entomology and Zoology · Cited by 7,268 · see citing works
Predictive reward signal of dopamine neurons
Schultz, W. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.1.1 · Cited by 4,564 · see citing works
Self-citationOngur, D. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.206 · Cited by 2,627 · see citing works
Neuron Activity Related to Short-Term Memory
Fuster, J. M., & Alexander, G. E. (1971) · Science · doi:10.1126/science.173.3997.652 · Cited by 2,085 · see citing works
Wise, R. A., & Rompre, P.-P. (1989) · Annual Review of Psychology · doi:10.1146/annurev.ps.40.020189.001203 · Cited by 1,968 · see citing works
The Orbitofrontal Cortex and Reward
Rolls, E. T. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.284 · Cited by 1,595 · see citing works
Dissociation in prefrontal cortex of affective and attentional shifts
Dias, R., Robbins, T. W., & Roberts, A. C. (1996) · Nature · doi:10.1038/380069a0 · Cited by 1,527 · see citing works
Toward a modern theory of adaptive networks: Expectation and prediction.
Sutton, R. S., & Barto, A. G. (1981) · Psychological Review · doi:10.1037/0033-295x.88.2.135 · Cited by 1,450 · see citing works
Dissociation of object and spatial processing domains in primate prefrontal cortex.
Wilson, F. A., Scalaidhe, S. P. Ó., & Goldman-Rakic, P. (1993) · Science · doi:10.1126/science.8316836 · Cited by 1,374 · see citing works
Relative reward preference in primate orbitofrontal cortex
Tremblay, L., & Schultz, W. (1999) · Nature · doi:10.1038/19525 · Cited by 1,314 · see citing works
Self-citationSchultz, W., Apicella, P., & Ljungberg, T. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-03-00900.1993 · Cited by 1,291 · see citing works
Self-citationLimbic connections of the orbital and medial prefrontal cortex in macaque monkeys
Carmichael, S. T., & Price, J. L. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903630408 · Cited by 1,197 · see citing works
Neurobehavioural mechanisms of reward and motivation
Robbins, T. W., & Everitt, B. J. (1996) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(96)80077-8 · Cited by 1,187 · see citing works
Dopamine neurons report an error in the temporal prediction of reward during learning
Hollerman, J. R., & Schultz, W. (1998) · Nature Neuroscience · doi:10.1038/1124 · Cited by 1,103 · see citing works
Self-citationLongitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey
Selemon, L. D., & Goldman-Rakic, P. S. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-03-00776.1985 · Cited by 1,074 · see citing works
Wise, R. A. (1996) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(96)80079-1 · Cited by 1,072 · see citing works
Dissociation Of Working Memory from Decision Making within the Human Prefrontal Cortex
Bechara, A., Damásio, H., Tranel, D., & Anderson, S. W. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00428.1998 · Cited by 1,059 · see citing works
Fuster, J. M. (1973) · Journal of Neurophysiology · doi:10.1152/jn.1973.36.1.61 · Cited by 995 · see citing works
Motivational control of goal-directed action
Dickinson, A., & Balleine, B. (1994) · Animal Learning & Behavior · doi:10.3758/bf03199951 · Cited by 995 · see citing works
Responses of monkey dopamine neurons during learning of behavioral reactions
Ljungberg, T., Apicella, P., & Schultz, W. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.1.145 · Cited by 987 · see citing works
Self-citationThe Anatomical Connections of the Macaque Monkey Orbitofrontal Cortex. A Review
Cavada, C. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.220 · Cited by 917 · see citing works
Integration of What and Where in the Primate Prefrontal Cortex
Rao, S. C., Rainer, G., & Miller, E. K. (1997) · Science · doi:10.1126/science.276.5313.821 · Cited by 877 · see citing works
Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning
Schoenbaum, G. M., Chiba, A. A., & Gallagher, M. (1998) · Nature Neuroscience · doi:10.1038/407 · Cited by 849 · see citing works
The orbitofrontal cortex: Neuronal activity in the behaving monkey
Thorpe, S. J., Rolls, E. T., & Maddison, S. (1983) · Experimental Brain Research · doi:10.1007/bf00235545 · Cited by 836 · see citing works
Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli
Mirenowicz, J., & Schultz, W. (1996) · Nature · doi:10.1038/379449a0 · Cited by 829 · see citing works
Self-citationIversen, S., & Mishkin, M. (1970) · Experimental Brain Research · doi:10.1007/bf00237911 · Cited by 765 · see citing works
Rolls, E. T. (1996) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1996.0128 · Cited by 755 · see citing works
Alexander, G. E., & Crutcher, M. D. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.64.1.133 · Cited by 750 · see citing works
Neuronal activity in monkey ventral striatum related to the expectation of reward
Schultz, W., Apicella, P., Scarnati, E., & Ljungberg, T. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-12-04595.1992 · Cited by 744 · see citing works
Self-citationPrefrontal cortical unit activity and delayed alternation performance in monkeys.
Kubota, K., & Niki, H. (1971) · Journal of Neurophysiology · doi:10.1152/jn.1971.34.3.337 · Cited by 717 · see citing works
Reward expectancy in primate prefrental neurons
Watanabe, M. (1996) · Nature · doi:10.1038/382629a0 · Cited by 684 · cited 2× · see citing works
“Similar activities have been reported for the dorsolateral prefrontal cortex (Watanabe, 1996).”
BackgroundPrefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task
Funahashi, S., Chafee, M. V., & Goldman, P. S. (1993) · Nature · doi:10.1038/365753a0 · Cited by 662 · see citing works
A neural system for human visual working memory
Ungerleider, L. G., Courtney, S. M., & Haxby, J. V. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.3.883 · Cited by 654 · see citing works
Role for Cingulate Motor Area Cells in Voluntary Movement Selection Based on Reward
Shima, K., & Tanji, J. (1998) · Science · doi:10.1126/science.282.5392.1335 · Cited by 653 · see citing works
Expectation of reward modulates cognitive signals in the basal ganglia
Kawagoe, R., Takikawa, Y., & Hikosaka, O. (1998) · Nature Neuroscience · doi:10.1038/1625 · Cited by 632 · see citing works
The orbital and medial prefrontal circuit through the primate basal ganglia
Haber, S., Kunishio, K., Mizobuchi, M., & Lynd-Balta, E. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-07-04851.1995 · Cited by 605 · see citing works
Hikosaka, O., Sakamoto, M., & Usui, S. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.4.814 · Cited by 579 · see citing works
Behavioral effects of selective ablation of the caudate nucleus.
Divac, I., Rosvold, H. E., & Szwarcbart, M. K. (1967) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0024348 · Cited by 568 · see citing works
Petrides, M., & Pandya, D. Ν. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902730106 · Cited by 547 · see citing works
Importance of unpredictability for reward responses in primate dopamine neurons
Mirenowicz, J., & Schultz, W. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.72.2.1024 · Cited by 544 · see citing works
Self-citationFunctional properties of monkey caudate neurons. I. Activities related to saccadic eye movements
Hikosaka, O., Sakamoto, M., & Usui, S. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.4.780 · Cited by 533 · see citing works
Barbas, H. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902760302 · Cited by 515 · see citing works
Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms
Funahashi, S., Bruce, C. J., & Goldman‐Rakic, P. S. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.4.814 · Cited by 443 · see citing works
Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey
Eblen, F., & Graybiel, A. M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-09-05999.1995 · Cited by 391 · see citing works
Influence of Reward Expectation on Behavior-Related Neuronal Activity in Primate Striatum
Hollerman, J. R., Tremblay, L., & Schultz, W. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.2.947 · Cited by 380 · see citing works
Self-citationSingle cell studies of the primate putamen
Crutcher, M. D., & DeLong, M. R. (1984) · Experimental Brain Research · doi:10.1007/bf00238153 · Cited by 379 · see citing works
Owen, A. M., Stern, C. E., Look, R. B., Tracey, I., Rosen, B. R., & Petrides, M. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.13.7721 · Cited by 372 · see citing works
Responses to reward in monkey dorsal and ventral striatum
Apicella, P., Ljungberg, T., Scarnati, E., & Schultz, W. (1991) · Experimental Brain Research · doi:10.1007/bf00231732 · Cited by 369 · see citing works
Self-citationRomo, R., & Schultz, W. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.3.592 · Cited by 353 · cited 4× · see citing works
“Hollerman and Schultz, 1998) and when touching food during self-initiated movements (Romo and Schultz, 1990).”
BackgroundInfluentialSelf-citationHikosaka, K. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.263 · Cited by 345 · see citing works
Nishijo, H., Ono, T., & Nishino, H. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-10-03570.1988 · Cited by 333 · see citing works
Crutcher, M. D., & Alexander, G. E. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.64.1.151 · Cited by 331 · see citing works
Neuronal activity in monkey striatum related to the expectation of predictable environmental events
Apicella, P., Scarnati, E., Ljungberg, T., & Schultz, W. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.3.945 · Cited by 305 · see citing works
Self-citationHaber, S. N., Lynd‐Balta, E., Klein, C. M., & Groenewegen, H. J. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902930210 · Cited by 291 · see citing works
Reward-Related Neuronal Activity During Go-Nogo Task Performance in Primate Orbitofrontal Cortex
Tremblay, L., & Schultz, W. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.4.1864 · Cited by 287 · see citing works
Self-citationSingle cell studies of the primate putamen
Crutcher, M. D., & DeLong, M. R. (1984) · Experimental Brain Research · doi:10.1007/bf00238154 · Cited by 283 · see citing works
Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey
Rolls, E. T., Yaxley, S., & Sienkiewicz, Z. J. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.64.4.1055 · Cited by 282 · see citing works
Role of primate basal ganglia and frontal cortex in the internal generation of movements
Romo, R., & Schultz, W. (1992) · Experimental Brain Research · doi:10.1007/bf00227836 · Cited by 271 · see citing works
Self-citationModifications of Reward Expectation-Related Neuronal Activity During Learning in Primate Striatum
Tremblay, L., Hollerman, J. R., & Schultz, W. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.2.964 · Cited by 267 · see citing works
Self-citationRole of primate basal ganglia and frontal cortex in the internal generation of movements
Romo, R., Scarnati, E., & Schultz, W. (1992) · Experimental Brain Research · doi:10.1007/bf00227835 · Cited by 266 · see citing works
Self-citationNader, M. A., & Woolverton, W. L. (1991) · Psychopharmacology · doi:10.1007/bf02244304 · Cited by 253 · see citing works
Object-Centered Direction Selectivity in the Macaque Supplementary Eye Field
Olson, C. R., & Gettner, S. N. (1995) · Science · doi:10.1126/science.7638625 · Cited by 238 · see citing works
Single cell activity in ventral prefrontal cortex of behaving monkeys
Rosenkilde, C. E., Bauer, R. H., & Fuster, J. M. (1981) · Brain Research · doi:10.1016/0006-8993(81)90160-8 · Cited by 233 · see citing works
Shidara, M., Aigner, T. G., & Richmond, B. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-07-02613.1998 · Cited by 205 · see citing works
Reward, Motivation, Cognition: Psychobiology of Mesotelencephalic Dopamine Systems
Fibiger, H. C., & Phillips, A. G. (1986) · Comprehensive physiology · doi:10.1002/cphy.cp010412 · Cited by 204 · see citing works
Critchley, H., & Rolls, E. T. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.4.1659 · Cited by 190 · see citing works
Tremblay, L., & Schultz, W. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.4.1877 · Cited by 167 · see citing works
Self-citationBaylis, L. L., & Gaffan, D. (1991) · Experimental Brain Research · doi:10.1007/bf00230535 · Cited by 166 · see citing works
Visuokinetic activities of primate prefrontal neurons during delayed-response performance.
Kubota, K., Iwamoto, T., & Suzuki, H. (1974) · Journal of Neurophysiology · doi:10.1152/jn.1974.37.6.1197 · Cited by 162 · see citing works
Jacobsen, C. F., & Nissen, H. W. (1937) · Journal of comparative psychology · doi:10.1037/h0056632 · Cited by 160 · see citing works
Prefrontal unit activity during associative learning in the monkey
Watanabe, M. (1990) · Experimental Brain Research · doi:10.1007/bf00228157 · Cited by 149 · see citing works
Frontal units of the monkey coding the associative significance of visual and auditory stimuli
Watanabe, M. (1992) · Experimental Brain Research · doi:10.1007/bf00228241 · Cited by 123 · see citing works
Species recognition by five macaque monkeys
Fujita, K. (1987) · Primates · doi:10.1007/bf02381018 · Cited by 115 · see citing works
Context-dependent Activity in Primate Striatum Reflecting Past and Future Behavioral Events
Schultz, W., Apicella, P., Romo, R., & Scarnati, E. (1994) · The MIT Press eBooks · doi:10.7551/mitpress/4708.003.0005 · Cited by 113 · see citing works
Self-citationThe role of the basal ganglia in controlling a movement initiated by a visually presented cue
Aldridge, J. W., Anderson, R. J., & Murphy, J. T. (1980) · Brain Research · doi:10.1016/0006-8993(80)91003-3 · Cited by 83 · see citing works
The striatum and motor cortex in motor initiation and execution
Montgomery, E. B., & Buchholz, S. R. (1991) · Brain Research · doi:10.1016/0006-8993(91)90461-4 · Cited by 58 · see citing works
Perceived control in rhesus monkeys (Macaca mulatta): Enhanced video-task performance.
Washburn, D. A., Hopkins, W. D., & Rumbaugh, D. M. (1991) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.17.2.123 · Cited by 54 · see citing works
Gardiner, T. W., & Nelson, R. J. (1992) · Experimental Brain Research · doi:10.1007/bf00230379 · Cited by 48 · see citing works
Johnstone, S., & Rolls, E. T. (1990) · Brain Research · doi:10.1016/0006-8993(90)91591-4 · Cited by 46 · see citing works
REWARD DISCRIMINATION IN PRIMATE STRIATUM
Cromwell, H. C., Hassani, O. K., & Schultz, W. (1998) · Behavioural Pharmacology · doi:10.1097/00008877-199808000-00043 · Cited by 6 · see citing works
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Sorted by citations
Aston-Jones, G., & Cohen, J. D. (2005) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135709 · Cited by 4,472 · see citing works
The reward circuit: linking primate anatomy and human imaging
Haber, S. N., & Knutson, B. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.129 · Cited by 3,718 · see citing works
Goldstein, R. Z., & Volkow, N. D. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.10.1642 · Cited by 2,667 · see citing works
Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens
Knutson, B., Adams, C. M., Fong, G. W., & Hommer, D. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-16-j0002.2001 · Cited by 2,244 · see citing works
Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex
Cardinal, R. N., Parkinson, J. A., Hall, J., & Everitt, B. J. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(02)00007-6 · Cited by 2,129 · see citing works
The somatic marker hypothesis: A neural theory of economic decision
Bechara, A., & Damasio, A. R. (2005) · Games and Economic Behavior · doi:10.1016/j.geb.2004.06.010 · Cited by 1,986 · see citing works
Effects of Attention and Emotion on Face Processing in the Human Brain
Vuilleumier, P., Armony, J. L., Driver, J., & Dolan, R. J. (2001) · Neuron · doi:10.1016/s0896-6273(01)00328-2 · Cited by 1,664 · see citing works
Neural Mechanisms for Interacting with a World Full of Action Choices
Cisek, P., & Kalaska, J. F. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135409 · Cited by 1,543 · see citing works
The primate basal ganglia: Parallel and integrative networks
Haber, S. N. (2003) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2003.10.003 · Cited by 1,479 · see citing works
A neural basis for social cooperation
Rilling, J. K., Gutman, D. A., Zeh, T. R., Pagnoni, G., Berns, G. S., & Kilts, C. D. (2002) · Neuron · doi:10.1016/s0896-6273(02)00755-9 · Cited by 1,451 · see citing works
Barrett, L. F., Mesquita, B., Ochsner, K. N., & Gross, J. J. (2007) · Annual Review of Psychology · doi:10.1146/annurev.psych.58.110405.085709 · Cited by 1,425 · see citing works
The functions of the orbitofrontal cortex
Rolls, E. T. (2004) · Brain and Cognition · doi:10.1016/s0278-2626(03)00277-x · Cited by 1,327 · see citing works
Dissociation of reward anticipation and outcome with event-related fMRI
Knutson, B., Fong, G. W., Adams, C. M., Varner, J. L., & Hommer, D. (2001) · Neuroreport · doi:10.1097/00001756-200112040-00016 · Cited by 1,300 · see citing works
Neural mechanisms of autonomic, affective, and cognitive integration
Critchley, H. D. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20749 · Cited by 1,214 · see citing works
Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex
Gottfried, J. A., O'Doherty, J., & Dolan, R. J. (2003) · Science · doi:10.1126/science.1087919 · Cited by 1,165 · see citing works
Kober, H., Barrett, L. F., Joseph, J., Bliss-Moreau, E., Lindquist, K., & Wager, T. D. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.03.059 · Cited by 1,144 · see citing works
The Psychobiology of Depression and Resilience to Stress: Implications for Prevention and Treatment
Southwick, S. M., Vythilingam, M., & Charney, D. S. (2005) · Annual Review of Clinical Psychology · doi:10.1146/annurev.clinpsy.1.102803.143948 · Cited by 1,160 · see citing works
Functional connectivity of human striatum: a resting state FMRI study
Di Martino, A., Scheres, A., Margulies, D. S., Kelly, A. M. C., Uddin, L. Q., Shehzad, Z., Biswal, B., Walters, J. R., Castellanos, F. X., & Milham, M. P. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn041 · Cited by 1,090 · see citing works
Dopamine in drug abuse and addiction: results from imaging studies and treatment implications
Volkow, N. D., Fowler, J. S., Wang, G.-J., & Swanson, J. M. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001507 · Cited by 1,101 · see citing works
Neural responses during anticipation of a primary taste reward
O'Doherty, J. P., Deichmann, R., Critchley, H. D., & Dolan, R. J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00603-7 · Cited by 1,076 · see citing works
Imaging dopamine's role in drug abuse and addiction
Volkow, N. D., Fowler, J. S., Wang, G. J., Baler, R., & Telang, F. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.05.022 · Cited by 988 · see citing works
Complementary roles of basal ganglia and cerebellum in learning and motor control
Doya, K. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00153-7 · Cited by 964 · see citing works
Temperament and developmental psychopathology
Nigg, J. T. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01612.x · Cited by 971 · see citing works
Architectonic subdivision of the human orbital and medial prefrontal cortex
Öngür, D., Ferry, A. T., & Price, J. L. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10609 · Cited by 944 · see citing works
Coherent spontaneous activity identifies a hippocampal-parietal memory network
Vincent, J. L., Snyder, A. Z., Fox, M. D., Shannon, B. J., Andrews, J. R., Raichle, M. E., & Buckner, R. L. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00048.2006 · Cited by 959 · see citing works
Cools, R. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.12.1136 · Cited by 906 · see citing works
Impulsive choice induced in rats by lesions of the nucleus accumbens core
Cardinal, R. N., Pennicott, D. R., Lakmali, C., Sugathapala, Robbins, T. W., & Everitt, B. J. (2001) · Science · doi:10.1126/science.1060818 · Cited by 923 · see citing works
Liu, X., Hairston, J., Schrier, M., & Fan, J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.12.012 · Cited by 916 · see citing works
Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness
O’Doherty, J., Winston, J., Critchley, H., Perrett, D., Burt, D. M., & Dolan, R. J. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(02)00145-8 · Cited by 898 · see citing works
The addicted human brain: insights from imaging studies
Volkow, N. D., Fowler, J. S., & Wang, G.-J. (2003) · Journal of Clinical Investigation · doi:10.1172/jci18533 · Cited by 916 · see citing works
Processing of Social and Monetary Rewards in the Human Striatum
Izuma, K., Saito, D. N., & Sadato, N. (2008) · Neuron · doi:10.1016/j.neuron.2008.03.020 · Cited by 855 · see citing works
New insights into symptoms and neurocircuit function of anorexia nervosa
Kaye, W. H., Fudge, J. L., & Paulus, M. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2682 · Cited by 843 · see citing works
Kringelbach, M. L. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.10.1064 · Cited by 824 · see citing works
Eye guidance in natural vision: reinterpreting salience
Tatler, B. W., Hayhoe, M. M., Land, M. F., & Ballard, D. H. (2011) · Journal of Vision · doi:10.1167/11.5.5 · Cited by 775 · see citing works
Limbic-frontal circuitry in major depression: a path modeling metanalysis
Seminowicz, D. A., Mayberg, H. S., McIntosh, A. R., Goldapple, K., Kennedy, S., Segal, Z., & Rafi-Tari, S. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.01.015 · Cited by 710 · see citing works
Haber, S. N., Kim, K.-S., Mailly, P., & Calzavara, R. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0271-06.2006 · Cited by 686 · see citing works
Hierarchically organized behavior and its neural foundations: A reinforcement learning perspective
Botvinick, M. M., Niv, Y., & Barto, A. G. (2009) · Cognition · doi:10.1016/j.cognition.2008.08.011 · Cited by 646 · see citing works
Fox, K. C. R., Dixon, M. L., Nijeboer, S., Girn, M., Floman, J. L., Lifshitz, M., Ellamil, M., Sedlmeier, P., & Christoff, K. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.03.021 · Cited by 656 · see citing works
Social dominance in monkeys: dopamine D2 receptors and cocaine self-administration
Morgan, D., Grant, K. A., Gage, H. D., Mach, R. H., Kaplan, J. R., Prioleau, O., Nader, S. H., Buchheimer, N., Ehrenkaufer, R. L., & Nader, M. A. (2002) · Nature Neuroscience · doi:10.1038/nn798 · Cited by 674 · see citing works
Doya, K. (2008) · Nature Neuroscience · doi:10.1038/nn2077 · Cited by 642 · see citing works
Neurobiology of anorexia and bulimia nervosa
Kaye, W. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.11.037 · Cited by 625 · see citing works
NIGG, J. T., & CASEY, B. J. (2005) · Development and Psychopathology · doi:10.1017/s0954579405050376 · Cited by 593 · see citing works
Inflammation-Induced Anhedonia: Endotoxin Reduces Ventral Striatum Responses to Reward
Eisenberger, N. I., Berkman, E. T., Inagaki, T. K., Rameson, L. T., Mashal, N. M., & Irwin, M. R. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.06.010 · Cited by 596 · see citing works
Cortex and memory: emergence of a new paradigm
Fuster, J. M. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21280 · Cited by 559 · see citing works
Neurobiologic processes in drug reward and addiction
Adinoff, B. (2004) · Harvard Review of Psychiatry · doi:10.1080/10673220490910844 · Cited by 546 · see citing works
Frontostriatal maturation predicts cognitive control failure to appetitive cues in adolescents
Somerville, L. H., Hare, T., & Casey, B. J. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21572 · Cited by 523 · see citing works
Volkow, N. D., Wang, G., Fowler, J. S., Tomasi, D., Telang, F., & Baler, R. (2010) · BioEssays · doi:10.1002/bies.201000042 · Cited by 532 · see citing works
The free-energy self: a predictive coding account of self-recognition
Apps, M. A. J., & Tsakiris, M. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.01.029 · Cited by 514 · see citing works
Cools, R., Barker, R. A., Sahakian, B. J., & Robbins, T. W. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(03)00117-9 · Cited by 516 · see citing works
Volkow, N. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4099 · Cited by 514 · see citing works
Neural systems and cue-induced cocaine craving
Bonson, K. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00371-2 · Cited by 507 · see citing works
The neurobiology of pathological gambling and drug addiction: an overview and new findings
Potenza, M. N. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2008.0100 · Cited by 508 · see citing works
Actor–critic models of the basal ganglia: new anatomical and computational perspectives
Joel, D., Niv, Y., & Ruppin, E. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00047-3 · Cited by 500 · see citing works
Learning and selective attention
Dayan, P., Kakade, S., & Montague, P. R. (2000) · Nature Neuroscience · doi:10.1038/81504 · Cited by 495 · see citing works
Placebo and the New Physiology of the Doctor-Patient Relationship
Benedetti, F. (2013) · Physiological Reviews · doi:10.1152/physrev.00043.2012 · Cited by 492 · see citing works
Human hippocampal theta oscillations and the formation of episodic memories
Lega, B. C., Jacobs, J., & Kahana, M. (2012) · Hippocampus · doi:10.1002/hipo.20937 · Cited by 485 · see citing works
Beer, J. S., John, O. P., Scabini, D., & Knight, R. T. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.6.871 · Cited by 455 · see citing works
Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans
Small, D. M., Gerber, J. C., Mak, Y. E., & Hummel, T. (2005) · Neuron · doi:10.1016/j.neuron.2005.07.022 · Cited by 463 · see citing works
PRICE, J. L. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1401.008 · Cited by 395 · see citing works
The orbitofrontal-amygdala circuit and self-regulation of social-emotional behavior in autism
Bachevalier, J., & Loveland, K. A. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.07.002 · Cited by 402 · see citing works
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 · see citing works
Choice selection and reward anticipation: an fMRI study
Ernst, M., Nelson, E. E., McClure, E. B., Monk, C. S., Munson, S., Eshel, N., Zarahn, E., Leibenluft, E., Zametkin, A., Towbin, K., et al. (2004) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.05.011 · Cited by 377 · see citing works
Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants
Nitschke, J. B., Nelson, E. E., Rusch, B. D., Fox, A. S., Oakes, T. R., & Davidson, R. J. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.10.005 · Cited by 371 · see citing works
The neural bases of obsessive-compulsive disorder in children and adults
Maia, T. V., Cooney, R. E., & Peterson, B. S. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000606 · Cited by 362 · see citing works
Attention-Deficit/Hyperactivity Disorder and Attention Networks
Bush, G. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.120 · Cited by 358 · see citing works
Rilling, J. K., DeMarco, A. C., Hackett, P. D., Chen, X., Gautam, P., Stair, S., Haroon, E., Thompson, R., Ditzen, B., Patel, R., et al. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.09.022 · Cited by 343 · see citing works
“Given the role of the ventral striatum in reward processing (Knutson et al., 2005; O’Doherty, 2004; Schultz et al., 2000), these results suggest that intranasal OT may augment the experienced (player 1) or anticipated (player 2) reward from mutual cooperation between men but not between women.”
Meyer, B., Johnson, S. L., & Winters, R. (2001) · Journal of Psychopathology and Behavioral Assessment · doi:10.1023/a:1010929402770 · Cited by 326 · see citing works
Saleem, K. S., Kondo, H., & Price, J. L. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21577 · Cited by 315 · see citing works
Reward, Addiction, and Emotion Regulation Systems Associated With Rejection in Love
Fisher, H. E., Brown, L. L., Aron, A., Strong, G., & Mashek, D. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00784.2009 · Cited by 328 · see citing works
Bari, A., Theobald, D. E., Caprioli, D., Mar, A. C., Aidoo-Micah, A., Dalley, J. W., & Robbins, T. W. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.233 · Cited by 325 · see citing works
Dysfunctional reward circuitry in obsessive-compulsive disorder
Figee, M., Vink, M., de Geus, F., Vulink, N., Veltman, D. J., Westenberg, H., & Denys, D. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.12.003 · Cited by 315 · see citing works
Wahlstrom, D., Collins, P., White, T., & Luciana, M. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.10.013 · Cited by 311 · see citing works
Enhanced Striatal Dopamine Release During Food Stimulation in Binge Eating Disorder
Wang, G., Geliebter, A., Volkow, N. D., Telang, F. W., Logan, J., Jayne, M. C., Galanti, K., Selig, P. A., Han, H., Zhu, W., et al. (2011) · Obesity · doi:10.1038/oby.2011.27 · Cited by 313 · see citing works
Volkow, N. D., Wang, G.-J., Ma, Y., Fowler, J. S., Zhu, W., Maynard, L., Telang, F., Vaska, P., Ding, Y.-S., Wong, C., et al. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-36-11461.2003 · Cited by 302 · see citing works
Mother–infant bonding and the evolution of mammalian social relationships
Broad, K. D., Curley, J. P., & Keverne, E. B. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1940 · Cited by 283 · see citing works
Processing of the incentive for social approval in the ventral striatum during charitable donation
Izuma, K., Saito, D. N., & Sadato, N. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21228 · Cited by 276 · see citing works
Wagner, A., Aizenstein, H., Mazurkewicz, L., Fudge, J., Frank, G. K., Putnam, K., Bailer, U. F., Fischer, L., & Kaye, W. H. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301443 · Cited by 261 · see citing works
The role of the brain reward system in depression
Naranjo, C. A., Tremblay, L. K., & Busto, U. E. (2001) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(01)00156-7 · Cited by 245 · see citing works
Motivation-dependent responses in the human caudate nucleus.
Delgado, M. R. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh062 · Cited by 246 · see citing works
Kondo, H., Saleem, K. S., & Price, J. L. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20796 · Cited by 236 · see citing works
Striatal mechanisms underlying movement, reinforcement, and punishment
Kravitz, A. V., & Kreitzer, A. C. (2012) · Physiology · doi:10.1152/physiol.00004.2012 · Cited by 224 · see citing works
From prediction error to psychosis: Ketamine as a pharmacological model of delusions
Corlett, P. R., Honey, G. D., & Fletcher, P. C. (2007) · Journal of Psychopharmacology · doi:10.1177/0269881107077716 · Cited by 227 · see citing works
The maturation of incentive processing and cognitive control
Geier, C., & Luna, B. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.01.021 · Cited by 225 · see citing works
Predictability modulates the affective and sensory-discriminative neural processing of pain
Carlsson, K., Andersson, J., Petrovic, P., Petersson, K. M., Öhman, A., & Ingvar, M. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.05.027 · Cited by 208 · see citing works
The prefrontal cortex and working memory: physiology and brain imaging
Passingham, D., & Sakai, K. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.003 · Cited by 207 · see citing works
Padmanabhan, 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 · see citing works
Waiting to perceive: Reward or punishment?
Brunia, C. H. M., Hackley, S. A., van Boxtel, G. J. M., Kotani, Y., & Ohgami, Y. (2011) · Clinical Neurophysiology · doi:10.1016/j.clinph.2010.12.039 · Cited by 176 · see citing works
The role of emotion in pain modulation.
Rhudy, J. L., & Meagher, M. W. (2001) · Current Opinion in Psychiatry · doi:10.1097/00001504-200105000-00012 · Cited by 170 · see citing works
Luciana, M., Wahlstrom, D., Porter, J. N., & Collins, P. F. (2012) · Developmental Psychology · doi:10.1037/a0027432 · Cited by 156 · see citing works
Face-selective and auditory neurons in the primate orbitofrontal cortex
Rolls, E. T., Critchley, H. D., Browning, A. S., & Inoue, K. (2006) · Experimental Brain Research · doi:10.1007/s00221-005-0191-y · Cited by 151 · see citing works
Neural responses to acute cocaine administration in the human brain detected by fMRI
Kufahl, P. R., Li, Z., Risinger, R. C., Rainey, C. J., Wu, G., Bloom, A. S., & Li, S.-J. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.06.039 · Cited by 151 · see citing works
Aerobic exercise reduces neuronal responses in food reward brain regions
Evero, N., Hackett, L. C., Clark, R. D., Phelan, S., & Hagobian, T. A. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01365.2011 · Cited by 150 · see citing works
Reward-related processing in the human brain: developmental considerations
Fareri, D. S., Martin, L. N., & Delgado, M. R. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000576 · Cited by 141 · see citing works
Zhu, J., & Reith, M. (2008) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152708786927877 · Cited by 140 · see citing works
Setlow, B., Holland, P. C., & Gallagher, M. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.2.267 · Cited by 160 · see citing works
Dopamine D2 receptor availability and amphetamine-induced dopamine release in unipolar depression
Parsey, R. V., Oquendo, M. A., Zea-Ponce, Y., Rodenhiser, J., Kegeles, L. S., Pratap, M., Cooper, T. B., Van Heertum, R., Mann, J. J., & Laruelle, M. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01089-7 · Cited by 133 · see citing works
Thanos, P. K., Michaelides, M., Piyis, Y. K., Wang, G., & Volkow, N. D. (2008) · Synapse · doi:10.1002/syn.20468 · Cited by 135 · see citing works
Fox, K. C. R., Shi, L., Baek, S., Raccah, O., Foster, B. L., Saha, S., Margulies, D. S., Kucyi, A., & Parvizi, J. (2020) · Nature Human Behaviour · doi:10.1038/s41562-020-0910-1 · Cited by 133 · see citing works
Incentive Motivation, Cognitive Control, and the Adolescent Brain: Is It Time for a Paradigm Shift?
Luciana, M., & Collins, P. F. (2012) · Child Development Perspectives · doi:10.1111/j.1750-8606.2012.00252.x · Cited by 123 · see citing works
Reinforcement learning: Computational theory and biological mechanisms
Doya, K. (2007) · HFSP journal · doi:10.2976/1.2732246 · Cited by 150 · see citing works
- Authors
- Schultz, W.
- Affiliations
- University of Fribourg (CH)
- Corresponding author
- Schultz, W.
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2000-03-01
- Volume
- 10
- Issue
- 3
- Pages
- 272-283
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- OpenAlex
- W2111746164
- Cited by
- 942
- References
- 81
- Citations by year
- 2026: 7 · 2025: 10 · 2024: 17 · 2023: 14 · 2022: 34 · 2021: 21 · 2020: 23 · 2019: 23 · 2018: 29 · 2017: 33 · 2016: 34 · 2015: 35 · 2014: 43 · 2013: 42 · 2012: 50
- FWCI
- 21.60
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed (publishedVersion)
- reroDoc Digital Library (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- reward processing, orbitofrontal cortex, basal ganglia, striatum, nucleus accumbens, caudate nucleus, putamen, dopaminergic neurons, reward anticipation, reward prediction, delayed response task, motor preparation, prediction error, goal-directed behavior, primate neuroscience
- MeSH terms
- Animals, Basal Ganglia, Behavior, Animal, Dopamine, Electrophysiology, Frontal Lobe, Goals, Macaca fascicularis, Mental Processes, Neurons, Reward
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