Cerebral Cortex, Vol. 10, No. 3, 272-283,
March 2000
© 2000 Oxford University Press
Reward Processing in Primate Orbitofrontal Cortex and Basal Ganglia
Institute of Physiology and Program in Neuroscience, University of Fribourg, CH-1700 Fribourg, Switzerland
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.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  K. M. Cham, A. J. Anderson, and L. A. Abel Task-Induced Stress and Motivation Decrease Foveation-Period Durations in Infantile Nystagmus Syndrome Invest. Ophthalmol. Vis. Sci., July 1, 2008; 49(7): 2977 - 2984. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Cloutier, T. F. Heatherton, P. J. Whalen, and W. M. Kelley Are attractive people rewarding? Sex differences in the neural substrates of facial attractiveness. J. Cogn. Neurosci., June 1, 2008; 20(6): 941 - 951. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Minagawa-Kawai, S. Matsuoka, I. Dan, N. Naoi, K. Nakamura, and S. Kojima Prefrontal Activation Associated with Social Attachment: Facial-Emotion Recognition in Mothers and Infants Cereb Cortex, May 30, 2008; (2008) bhn081v1. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Z. Wheeler and L. K. Fellows The human ventromedial frontal lobe is critical for learning from negative feedback Brain, May 1, 2008; 131(5): 1323 - 1331. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Di Martino, A. Scheres, D.S. Margulies, A.M.C. Kelly, L.Q. Uddin, Z. Shehzad, B. Biswal, J.R. Walters, F.X. Castellanos, and M.P. Milham Functional Connectivity of Human Striatum: A Resting State fMRI Study Cereb Cortex, April 9, 2008; (2008) bhn041v1. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Bellebaum, B. Koch, M. Schwarz, and I. Daum Focal basal ganglia lesions are associated with impairments in reward-based reversal learning Brain, March 1, 2008; 131(3): 829 - 841. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. V. Kravitz and L. L. Peoples Background Firing Rates of Orbitofrontal Neurons Reflect Specific Characteristics of Operant Sessions and Modulate Phasic Responses to Reward-Associated Cues and Behavior J. Neurosci., January 23, 2008; 28(4): 1009 - 1018. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. L. PRICE Definition of the Orbital Cortex in Relation to Specific Connections with Limbic and Visceral Structures and Other Cortical Regions Ann. N.Y. Acad. Sci., December 1, 2007; 1121(1): 54 - 71. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. BARBAS Specialized Elements of Orbitofrontal Cortex in Primates Ann. N.Y. Acad. Sci., December 1, 2007; 1121(1): 10 - 32. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. J. EVERITT, D. M. HUTCHESON, K. D. ERSCHE, Y. PELLOUX, J. W. DALLEY, and T. W. ROBBINS The Orbital Prefrontal Cortex and Drug Addiction in Laboratory Animals and Humans Ann. N.Y. Acad. Sci., December 1, 2007; 1121(1): 576 - 597. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. SIMMONS, S. RAVEL, M. SHIDARA, and B. J. RICHMOND A Comparison of Reward-Contingent Neuronal Activity in Monkey Orbitofrontal Cortex and Ventral Striatum: Guiding Actions toward Rewards Ann. N.Y. Acad. Sci., December 1, 2007; 1121(1): 376 - 394. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. A. Kensinger, R. J. Garoff-Eaton, and D. L. Schacter How negative emotion enhances the visual specificity of a memory. J. Cogn. Neurosci., November 1, 2007; 19(11): 1872 - 1887. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. K. Fellows and M. J. Farah The Role of Ventromedial Prefrontal Cortex in Decision Making: Judgment under Uncertainty or Judgment Per Se? Cereb Cortex, November 1, 2007; 17(11): 2669 - 2674. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. D. Woolley, M. -L. Gorno-Tempini, W. W. Seeley, K. Rankin, S. S. Lee, B. R. Matthews, and B. L. Miller Binge eating is associated with right orbitofrontal-insular-striatal atrophy in frontotemporal dementia Neurology, October 2, 2007; 69(14): 1424 - 1433. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. S. N. Le, N. Pannacciulli, K. Chen, A. D Salbe, J. O Hill, R. R Wing, E. M Reiman, and J. Krakoff Less activation in the left dorsolateral prefrontal cortex in the reanalysis of the response to a meal in obese than in lean women and its association with successful weight loss Am. J. Clinical Nutrition, September 1, 2007; 86(3): 573 - 579. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Goel and R. J. Dolan Social regulation of affective experience of humor. J. Cogn. Neurosci., September 1, 2007; 19(9): 1574 - 1580. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P.R. Corlett, G.D. Honey, and P.C. Fletcher From prediction error to psychosis: ketamine as a pharmacological model of delusions J Psychopharmacol, May 1, 2007; 21(3): 238 - 252. [Abstract] [PDF]
|
|
|
|
|
|
D. LEE and H. SEO Mechanisms of Reinforcement Learning and Decision Making in the Primate Dorsolateral Prefrontal Cortex Ann. N.Y. Acad. Sci., May 1, 2007; 1104(1): 108 - 122. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. SAMEJIMA and K. DOYA Multiple Representations of Belief States and Action Values in Corticobasal Ganglia Loops Ann. N.Y. Acad. Sci., May 1, 2007; 1104(1): 213 - 228. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X. Liu, D. K. Powell, H. Wang, B. T. Gold, C. R. Corbly, and J. E. Joseph Functional Dissociation in Frontal and Striatal Areas for Processing of Positive and Negative Reward Information J. Neurosci., April 25, 2007; 27(17): 4587 - 4597. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. J. Freed and J. J. Mann Sadness and Loss: Toward a Neurobiopsychosocial Model Am J Psychiatry, January 1, 2007; 164(1): 28 - 34. [Full Text] [PDF]
|
|
|
|
 |
|
 J. L. Vincent, A. Z. Snyder, M. D. Fox, B. J. Shannon, J. R. Andrews, M. E. Raichle, and R. L. Buckner Coherent Spontaneous Activity Identifies a Hippocampal-Parietal Memory Network J Neurophysiol, December 1, 2006; 96(6): 3517 - 3531. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. S. N. Le, N. Pannacciulli, K. Chen, A. Del Parigi, A. D Salbe, E. M Reiman, and J. Krakoff Less activation of the left dorsolateral prefrontal cortex in response to a meal: a feature of obesity. Am. J. Clinical Nutrition, October 1, 2006; 84(4): 725 - 731. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. N. Haber, K.-S. Kim, P. Mailly, and R. Calzavara Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning. J. Neurosci., August 9, 2006; 26(32): 8368 - 8376. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Windmann, P. Kirsch, D. Mier, R. Stark, B. Walter, O. Gunturkun, and D. Vaitl On Framing Effects in Decision Making: Linking Lateral versus Medial Orbitofrontal Cortex Activation to Choice Outcome Processing. J. Cogn. Neurosci., July 1, 2006; 18(7): 1198 - 1211. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Levy and B. Dubois Apathy and the Functional Anatomy of the Prefrontal Cortex-Basal Ganglia Circuits Cereb Cortex, July 1, 2006; 16(7): 916 - 928. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Lehericy, E. Bardinet, L. Tremblay, P.-F. Van de Moortele, J.-B. Pochon, D. Dormont, D.-S. Kim, J. Yelnik, and K. Ugurbil Motor control in basal ganglia circuits using fMRI and brain atlas approaches Cereb Cortex, February 1, 2006; 16(2): 149 - 161. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Homayoun and B. Moghaddam Bursting of Prefrontal Cortex Neurons in Awake Rats is Regulated by Metabotropic Glutamate 5 (mGlu5) Receptors: Rate-dependent Influence and Interaction with NMDA Receptors Cereb Cortex, January 1, 2006; 16(1): 93 - 105. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. A. Winstanley, D. E.H. Theobald, J. W. Dalley, R. N. Cardinal, and T. W. Robbins Double Dissociation between Serotonergic and Dopaminergic Modulation of Medial Prefrontal and Orbitofrontal Cortex during a Test of Impulsive Choice Cereb Cortex, January 1, 2006; 16(1): 106 - 114. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. A. Koene and M. E. Hasselmo An Integrate-and-fire Model of Prefrontal Cortex Neuronal Activity during Performance of Goal-directed Decision Making Cereb Cortex, December 1, 2005; 15(12): 1964 - 1981. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Benedetti, H. S. Mayberg, T. D. Wager, C. S. Stohler, and J.-K. Zubieta Neurobiological Mechanisms of the Placebo Effect J. Neurosci., November 9, 2005; 25(45): 10390 - 10402. [Full Text] [PDF]
|
|
|
|
 |
|
 E. Azim, D. Mobbs, B. Jo, V. Menon, and A. L. Reiss Sex differences in brain activation elicited by humor PNAS, November 8, 2005; 102(45): 16496 - 16501. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Kawasaki, R. Adolphs, H. Oya, C. Kovach, H. Damasio, O. Kaufman, and M. Howard III Analysis of Single-Unit Responses to Emotional Scenes in Human Ventromedial Prefrontal Cortex J. Cogn. Neurosci., October 1, 2005; 17(10): 1509. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. R. Roesch and C. R. Olson Neuronal Activity in Primate Orbitofrontal Cortex Reflects the Value of Time J Neurophysiol, October 1, 2005; 94(4): 2457 - 2471. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. E. Hasselmo A Model of Prefrontal Cortical Mechanisms for Goal-directed Behavior J. Cogn. Neurosci., July 1, 2005; 17(7): 1115 - 1129. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Oya, R. Adolphs, H. Kawasaki, A. Bechara, A. Damasio, and M. A. Howard III Electrophysiological correlates of reward prediction error recorded in the human prefrontal cortex PNAS, June 7, 2005; 102(23): 8351 - 8356. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. M. L. Cox, A. Andrade, and I. S. Johnsrude Learning to Like: A Role for Human Orbitofrontal Cortex in Conditioned Reward J. Neurosci., March 9, 2005; 25(10): 2733 - 2740. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. J. Smith, S. Becker, and S. Kapur A Computational Model of the Functional Role of the Ventral-Striatal D2 Receptor in the Expression of Previously Acquired Behaviors Neural Comput., February 1, 2005; 17(2): 361 - 395. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Ogawa, H. Ifuku, T. Nakamura, and S. Hirata Possible Changes in Information from the Primary to Higher-order Gustatory Cortices, Studied by Recording Neural Activities during a Taste Discrimination GO/NOGO Task in Monkeys Chem Senses, January 1, 2005; 30(suppl_1): i78 - i79. [Full Text] [PDF]
|
|
|
|
 |
|
 M. Habib Athymhormia and Disorders of Motivation in Basal Ganglia Disease J Neuropsychiatry Clin Neurosci, November 1, 2004; 16(4): 509 - 524. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. O. Hjelmstad Dopamine Excites Nucleus Accumbens Neurons through the Differential Modulation of Glutamate and GABA Release J. Neurosci., September 29, 2004; 24(39): 8621 - 8628. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. P. Hasegawa, A. M. Blitz, and M. E. Goldberg Neurons in Monkey Prefrontal Cortex Whose Activity Tracks the Progress of a Three-Step Self-Ordered Task J Neurophysiol, September 1, 2004; 92(3): 1524 - 1535. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M.R. Delgado, V.A. Stenger, and J.A. Fiez Motivation-dependent Responses in the Human Caudate Nucleus Cereb Cortex, September 1, 2004; 14(9): 1022 - 1030. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Taverna, Y. C. van Dongen, H. J. Groenewegen, and C. M.A. Pennartz Direct Physiological Evidence for Synaptic Connectivity Between Medium-Sized Spiny Neurons in Rat Nucleus Accumbens In Situ J Neurophysiol, March 1, 2004; 91(3): 1111 - 1121. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. D. Volkow, G.-J. Wang, Y. Ma, J. S. Fowler, W. Zhu, L. Maynard, F. Telang, P. Vaska, Y.-S. Ding, C. Wong, et al. Expectation Enhances the Regional Brain Metabolic and the Reinforcing Effects of Stimulants in Cocaine Abusers J. Neurosci., December 10, 2003; 23(36): 11461 - 11468. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. DACKIS and C. O'BRIEN Glutamatergic Agents for Cocaine Dependence Ann. N.Y. Acad. Sci., November 1, 2003; 1003(1): 328 - 345. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Heimer A New Anatomical Framework for Neuropsychiatric Disorders and Drug Abuse Am J Psychiatry, October 1, 2003; 160(10): 1726 - 1739. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M.L. Kringelbach, J. O'Doherty, E.T. Rolls, and C. Andrews Activation of the Human Orbitofrontal Cortex to a Liquid Food Stimulus is Correlated with its Subjective Pleasantness Cereb Cortex, October 1, 2003; 13(10): 1064 - 1071. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. F. Zink, G. Pagnoni, M. E. Martin, M. Dhamala, and G. S. Berns Human Striatal Response to Salient Nonrewarding Stimuli J. Neurosci., September 3, 2003; 23(22): 8092 - 8097. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. A. Gottfried, J. O'Doherty, and R. J. Dolan Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex Science, August 22, 2003; 301(5636): 1104 - 1107. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Treyer, A. Buck, and A. Schnider Subcortical Loop Activation during Selection of Currently Relevant Memories J. Cogn. Neurosci., May 1, 2003; 15(4): 610 - 618. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. T. Bello, K. L. Sweigart, J. M. Lakoski, R. Norgren, and A. Hajnal Restricted feeding with scheduled sucrose access results in an upregulation of the rat dopamine transporter Am J Physiol Regulatory Integrative Comp Physiol, May 1, 2003; 284(5): R1260 - R1268. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. A. Gusnard, J. M. Ollinger, G. L. Shulman, C. R. Cloninger, J. L. Price, D. C. Van Essen, and M. E. Raichle Persistence and brain circuitry PNAS, March 18, 2003; 100(6): 3479 - 3484. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Schoenbaum, B. Setlow, S. L. Nugent, M. P. Saddoris, and M. Gallagher Lesions of Orbitofrontal Cortex and Basolateral Amygdala Complex Disrupt Acquisition of Odor-Guided Discriminations and Reversals Learn. Mem., March 1, 2003; 10(2): 129 - 140. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Z. Goldstein and N. D. Volkow Drug Addiction and Its Underlying Neurobiological Basis: Neuroimaging Evidence for the Involvement of the Frontal Cortex Am J Psychiatry, October 1, 2002; 159(10): 1642 - 1652. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. B. Pochon, R. Levy, P. Fossati, S. Lehericy, J. B. Poline, B. Pillon, D. Le Bihan, and B. Dubois The neural system that bridges reward and cognition in humans: An fMRI study PNAS, April 16, 2002; 99(8): 5669 - 5674. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Adolphs Recognizing emotion from facial expressions: psychological and neurological mechanisms. Behav Cogn Neurosci Rev, March 1, 2002; 1(1): 21 - 62. [Abstract] [PDF]
|
|
|
|
|
|
V. B. Penhune and J. Doyon Dynamic Cortical and Subcortical Networks in Learning and Delayed Recall of Timed Motor Sequences J. Neurosci., February 15, 2002; 22(4): 1397 - 1406. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. M. Perlstein, T. Elbert, and V. A. Stenger Dissociation in human prefrontal cortex of affective influences on working memory-related activity PNAS, January 24, 2002; (2002) 241650598. [Abstract] [Full Text] [PDF]
|
|
|
|
|