 |
The Journal of Neuroscience, August 27, 2003, 23(21):7931-7939
Previous Article | Next Article 
Dissociating Valence of Outcome from Behavioral Control in Human Orbital and Ventral Prefrontal Cortices
John O'Doherty,
Hugo Critchley,
Ralf Deichmann, and
Raymond J. Dolan
Wellcome Department of Imaging Neuroscience, Institute of Neurology,
London WC1N 3BG, United Kingdom
The precise role of orbitofrontal cortex (OFC) in affective processing is
still debated. One view suggests OFC represents stimulus reward value and
supports learning and relearning of stimulus-reward associations. An alternate
view implicates OFC in behavioral control after rewarding or punishing
feedback. To discriminate between these possibilities, we used event-related
functional magnetic resonance imaging in subjects performing a reversal task
in which, on each trial, selection of the correct stimulus led to a 70%
probability of receiving a monetary reward and a 30% probability of obtaining
a monetary punishment. The incorrect stimulus had the reverse contingency. In
one condition (choice), subjects had to choose which stimulus to select and
switch their response to the other stimulus once contingencies had changed. In
another condition (imperative), subjects had simply to track the currently
rewarded stimulus. In some regions of OFC and medial prefrontal cortex,
activity was related to valence of outcome, whereas in adjacent areas activity
was associated with behavioral choice, signaling maintenance of the current
response strategy on a subsequent trial. Caudolateral OFC-anterior insula was
activated by punishing feedback preceding a switch in stimulus in both the
choice and imperative conditions, indicating a possible role for this region
in signaling a change in reward contingencies. These results suggest
functional heterogeneity within the OFC, with a role for this region in
representing stimulus-reward values, signaling changes in reinforcement
contingencies and in behavioral control.
Key words: reward; instrumental learning; behavioral control; orbitofrontal cortex; event-related; fMRI
Received April 16, 2003;
revised May 29, 2003;
accepted June 26, 2003.
This article has been cited by other articles:

|
 |

|
 |
 
D. G. Ghahremani, J. Monterosso, J. D. Jentsch, R. M. Bilder, and R. A. Poldrack
Neural Components Underlying Behavioral Flexibility in Human Reversal Learning
Cereb Cortex,
November 13, 2009;
(2009)
bhp247v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. R. St. Onge and S. B. Floresco
Prefrontal Cortical Contribution to Risk-Based Decision Making
Cereb Cortex,
November 5, 2009;
(2009)
bhp250v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Wunderlich, A. Rangel, and J. P. O'Doherty
Neural computations underlying action-based decision making in the human brain
PNAS,
October 6, 2009;
106(40):
17199 - 17204.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Kell, K. Neumann, K. von Kriegstein, C. Posenenske, A. W. von Gudenberg, H. Euler, and A.-L. Giraud
How the brain repairs stuttering
Brain,
October 1, 2009;
132(10):
2747 - 2760.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. G. V. Mitchell, Q. Luo, S. B. Avny, T. Kasprzycki, K. Gupta, G. Chen, E. C. Finger, and R. J. R. Blair
Adapting to Dynamic Stimulus-Response Values: Differential Contributions of Inferior Frontal, Dorsomedial, and Dorsolateral Regions of Prefrontal Cortex to Decision Making
J. Neurosci.,
September 2, 2009;
29(35):
10827 - 10834.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Christakou, M. Brammer, V. Giampietro, and K. Rubia
Right Ventromedial and Dorsolateral Prefrontal Cortices Mediate Adaptive Decisions under Ambiguity by Integrating Choice Utility and Outcome Evaluation
J. Neurosci.,
September 2, 2009;
29(35):
11020 - 11028.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. van Duuren, G. van der Plasse, J. Lankelma, R. N. J. M. A. Joosten, M. G. P. Feenstra, and C. M. A. Pennartz
Single-Cell and Population Coding of Expected Reward Probability in the Orbitofrontal Cortex of the Rat
J. Neurosci.,
July 15, 2009;
29(28):
8965 - 8976.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Fujiwara, P. N. Tobler, M. Taira, T. Iijima, and K.-I. Tsutsui
Segregated and Integrated Coding of Reward and Punishment in the Cingulate Cortex
J Neurophysiol,
June 1, 2009;
101(6):
3284 - 3293.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. M. C. Lee, C. C. H. Chan, A. W. S. Leung, P. T. Fox, and J.-H. Gao
Sex-Related Differences in Neural Activity during Risk Taking: An fMRI Study
Cereb Cortex,
June 1, 2009;
19(6):
1303 - 1312.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Elliott, Z. Agnew, and J.F.W. Deakin
Hedonic and Informational Functions of the Human Orbitofrontal Cortex
Cereb Cortex,
May 12, 2009;
(2009)
bhp092v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Xue, Z. Lu, I. P. Levin, J. A. Weller, X. Li, and A. Bechara
Functional Dissociations of Risk and Reward Processing in the Medial Prefrontal Cortex
Cereb Cortex,
May 1, 2009;
19(5):
1019 - 1027.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Seo and D. Lee
Behavioral and Neural Changes after Gains and Losses of Conditioned Reinforcers
J. Neurosci.,
March 18, 2009;
29(11):
3627 - 3641.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Kazama and J. Bachevalier
Selective Aspiration or Neurotoxic Lesions of Orbital Frontal Areas 11 and 13 Spared Monkeys' Performance on the Object Discrimination Reversal Task
J. Neurosci.,
March 4, 2009;
29(9):
2794 - 2804.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Gregorios-Pippas, P. N. Tobler, and W. Schultz
Short-Term Temporal Discounting of Reward Value in Human Ventral Striatum
J Neurophysiol,
March 1, 2009;
101(3):
1507 - 1523.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Glascher, A. N. Hampton, and J. P. O'Doherty
Determining a Role for Ventromedial Prefrontal Cortex in Encoding Action-Based Value Signals During Reward-Related Decision Making
Cereb Cortex,
February 1, 2009;
19(2):
483 - 495.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. D. Ragland, R. Cools, M. Frank, D. A. Pizzagalli, A. Preston, C. Ranganath, and A. D. Wagner
CNTRICS Final Task Selection: Long-Term Memory
Schizophr Bull,
January 1, 2009;
35(1):
197 - 212.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Klucharev, A. Smidts, and G. Fernandez
Brain mechanisms of persuasion: how 'expert power' modulates memory and attitudes
Soc Cogn Affect Neurosci,
December 1, 2008;
3(4):
353 - 366.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Schiller, I. Levy, Y. Niv, J. E. LeDoux, and E. A. Phelps
From Fear to Safety and Back: Reversal of Fear in the Human Brain
J. Neurosci.,
November 5, 2008;
28(45):
11517 - 11525.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. B. Bissonette, G. J. Martins, T. M. Franz, E. S. Harper, G. Schoenbaum, and E. M. Powell
Double Dissociation of the Effects of Medial and Orbital Prefrontal Cortical Lesions on Attentional and Affective Shifts in Mice
J. Neurosci.,
October 29, 2008;
28(44):
11124 - 11130.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Xue, D. G. Ghahremani, and R. A. Poldrack
Neural Substrates for Reversing Stimulus-Outcome and Stimulus-Response Associations
J. Neurosci.,
October 29, 2008;
28(44):
11196 - 11204.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Petrovic, B. Pleger, B. Seymour, S. Kloppel, B. De Martino, H. Critchley, and R. J. Dolan
Blocking Central Opiate Function Modulates Hedonic Impact and Anterior Cingulate Response to Rewards and Losses
J. Neurosci.,
October 15, 2008;
28(42):
10509 - 10516.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R.J.R Blair
The amygdala and ventromedial prefrontal cortex: functional contributions and dysfunction in psychopathy
Phil Trans R Soc B,
August 12, 2008;
363(1503):
2557 - 2565.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. B. Rowe, L. Hughes, B. C. P. Ghosh, D. Eckstein, C. H. Williams-Gray, S. Fallon, R. A. Barker, and A. M. Owen
Parkinson's disease and dopaminergic therapy--differential effects on movement, reward and cognition
Brain,
August 1, 2008;
131(8):
2094 - 2105.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. X. COHEN
Neurocomputational mechanisms of reinforcement-guided learning in humans: A review
Cogn Affect Behav Neurosci,
June 1, 2008;
8(2):
113 - 125.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
E. A. CRONE, K. ZANOLIE, L. VAN LEIJENHORST, M. P. WESTENBERG, and S. A. R. B. ROMBOUTS
Neural mechanisms supporting flexible performance adjustment during development
Cogn Affect Behav Neurosci,
June 1, 2008;
8(2):
165 - 177.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
K. N. Ochsner, J. Zaki, J. Hanelin, D. H. Ludlow, K. Knierim, T. Ramachandran, G. H. Glover, and S. C. Mackey
Your pain or mine? Common and distinct neural systems supporting the perception of pain in self and other
Soc Cogn Affect Neurosci,
June 1, 2008;
3(2):
144 - 160.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. C. Finger, A. A. Marsh, D. G. Mitchell, M. E. Reid, C. Sims, S. Budhani, D. S. Kosson, G. Chen, K. E. Towbin, E. Leibenluft, et al.
Abnormal Ventromedial Prefrontal Cortex Function in Children With Psychopathic Traits During Reversal Learning
Arch Gen Psychiatry,
May 1, 2008;
65(5):
586 - 594.
[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]
|
 |
|

|
 |

|
 |
 
L. Clark, A. Bechara, H. Damasio, M. R. F. Aitken, B. J. Sahakian, and T. W. Robbins
Differential effects of insular and ventromedial prefrontal cortex lesions on risky decision-making
Brain,
May 1, 2008;
131(5):
1311 - 1322.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. M. C. Lee, A. W. S. Leung, P. T. Fox, J.-H. Gao, and C. C. H. Chan
Age-related differences in neural activities during risk taking as revealed by functional MRI
Soc Cogn Affect Neurosci,
March 1, 2008;
3(1):
7 - 15.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B.-M. Gu, J.-Y. Park, D.-H. Kang, S. J. Lee, S. Y. Yoo, H. J. Jo, C.-H. Choi, J.-M. Lee, and J. S. Kwon
Neural correlates of cognitive inflexibility during task-switching in obsessive-compulsive disorder
Brain,
January 1, 2008;
131(1):
155 - 164.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. M. Morcom, J. Li, and M. D. Rugg
Age Effects on the Neural Correlates of Episodic Retrieval: Increased Cortical Recruitment with Matched Performance
Cereb Cortex,
November 1, 2007;
17(11):
2491 - 2506.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Robbins and A. Roberts
Differential Regulation of Fronto-Executive Function by the Monoamines and Acetylcholine
Cereb Cortex,
September 1, 2007;
17(suppl_1):
i151 - i160.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. A. Murray, J. P. O'Doherty, and G. Schoenbaum
What We Know and Do Not Know about the Functions of the Orbitofrontal Cortex after 20 Years of Cross-Species Studies
J. Neurosci.,
August 1, 2007;
27(31):
8166 - 8169.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. van Duuren, F. A. N. Escamez, R. N.J.M.A. Joosten, R. Visser, A. B. Mulder, and C. M.A. Pennartz
Neural coding of reward magnitude in the orbitofrontal cortex of the rat during a five-odor olfactory discrimination task
Learn. Mem.,
June 11, 2007;
14(6):
446 - 456.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R.J Dolan
The human amygdala and orbital prefrontal cortex in behavioural regulation
Phil Trans R Soc B,
May 29, 2007;
362(1481):
787 - 799.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y Chudasama, J. Kralik, and E. Murray
Rhesus Monkeys with Orbital Prefrontal Cortex Lesions Can Learn to Inhibit Prepotent Responses in the Reversed Reward Contingency Task
Cereb Cortex,
May 1, 2007;
17(5):
1154 - 1159.
[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]
|
 |
|

|
 |

|
 |
 
V. V. Valentin, A. Dickinson, and J. P. O'Doherty
Determining the Neural Substrates of Goal-Directed Learning in the Human Brain
J. Neurosci.,
April 11, 2007;
27(15):
4019 - 4026.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. K. Watson, B. J. Matthews, and J. M. Allman
Brain Activation during Sight Gags and Language-Dependent Humor
Cereb Cortex,
February 1, 2007;
17(2):
314 - 324.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. N. Hampton and J. P. O'Doherty
Decoding the neural substrates of reward-related decision making with functional MRI
PNAS,
January 23, 2007;
104(4):
1377 - 1382.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. G. Campbell
The Best of a Bad Bunch: The Ventromedial Prefrontal Cortex and Dorsal Anterior Cingulate Cortex in Decision-Making
J. Neurosci.,
January 17, 2007;
27(3):
447 - 448.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. D. Critchley, P. A. Lewis, M. Orth, O. Josephs, R. Deichmann, M. R. Trimble, and R. J. Dolan
Vagus Nerve Stimulation for Treatment-Resistant Depression: Behavioral and Neural Effects on Encoding Negative Material
Psychosom Med,
January 1, 2007;
69(1):
17 - 22.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Hampshire and A. M. Owen
Fractionating Attentional Control Using Event-Related fMRI
Cereb Cortex,
December 1, 2006;
16(12):
1679 - 1689.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Blair, A. A. Marsh, J. Morton, M. Vythilingam, M. Jones, K. Mondillo, D. C. Pine, W. C. Drevets, and J. R. Blair
Choosing the Lesser of Two Evils, the Better of Two Goods: Specifying the Roles of Ventromedial Prefrontal Cortex and Dorsal Anterior Cingulate in Object Choice.
J. Neurosci.,
November 1, 2006;
26(44):
11379 - 11386.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. L. Remijnse, M. M. A. Nielen, A. J. L. M. van Balkom, D. C. Cath, P. van Oppen, H. B. M. Uylings, and D. J. Veltman
Reduced orbitofrontal-striatal activity on a reversal learning task in obsessive-compulsive disorder.
Arch Gen Psychiatry,
November 1, 2006;
63(11):
1225 - 1236.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. I. Hooker, L. T. Germine, R. T. Knight, and M. D'Esposito
Amygdala response to facial expressions reflects emotional learning.
J. Neurosci.,
August 30, 2006;
26(35):
8915 - 8922.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. N. Hampton, P. Bossaerts, and J. P. O'Doherty
The Role of the Ventromedial Prefrontal Cortex in Abstract State-Based Inference during Decision Making in Humans.
J. Neurosci.,
August 9, 2006;
26(32):
8360 - 8367.
[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]
|
 |
|

|
 |

|
 |
 
A. Galvan, T. A. Hare, C. E. Parra, J. Penn, H. Voss, G. Glover, and B. J. Casey
Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents.
J. Neurosci.,
June 21, 2006;
26(25):
6885 - 6892.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Nicotra, H. D. Critchley, C. J. Mathias, and R. J. Dolan
Emotional and autonomic consequences of spinal cord injury explored using functional brain imaging
Brain,
March 1, 2006;
129(3):
718 - 728.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. M. Small, D. Gitelman, K. Simmons, S. M. Bloise, T. Parrish, and M.-M. Mesulam
Monetary Incentives Enhance Processing in Brain Regions Mediating Top-down Control of Attention
Cereb Cortex,
December 1, 2005;
15(12):
1855 - 1865.
[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]
|
 |
|

|
 |

|
 |
 
H. F. Clarke, S. C. Walker, H. S. Crofts, J. W. Dalley, T. W. Robbins, and A. C. Roberts
Prefrontal Serotonin Depletion Affects Reversal Learning But Not Attentional Set Shifting
J. Neurosci.,
January 12, 2005;
25(2):
532 - 538.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. R. Ridderinkhof, M. Ullsperger, E. A. Crone, and S. Nieuwenhuis
The Role of the Medial Frontal Cortex in Cognitive Control
Science,
October 15, 2004;
306(5695):
443 - 447.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. K. Fellows
The Cognitive Neuroscience of Human Decision Making: A Review and Conceptual Framework
Behav Cogn Neurosci Rev,
September 1, 2004;
3(3):
159 - 172.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
D. M. Small, J. Voss, Y. E. Mak, K. B. Simmons, T. Parrish, and D. Gitelman
Experience-Dependent Neural Integration of Taste and Smell in the Human Brain
J Neurophysiol,
September 1, 2004;
92(3):
1892 - 1903.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. M. McClure, M. K. York, and P. R. Montague
The Neural Substrates of Reward Processing in Humans: The Modern Role of fMRI
Neuroscientist,
June 1, 2004;
10(3):
260 - 268.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
J. M. Bjork, B. Knutson, G. W. Fong, D. M. Caggiano, S. M. Bennett, and D. W. Hommer
Incentive-Elicited Brain Activation in Adolescents: Similarities and Differences from Young Adults
J. Neurosci.,
February 25, 2004;
24(8):
1793 - 1802.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Merali, L. Du, P. Hrdina, M. Palkovits, G. Faludi, M. O. Poulter, and H. Anisman
Dysregulation in the Suicide Brain: mRNA Expression of Corticotropin-Releasing Hormone Receptors and GABAA Receptor Subunits in Frontal Cortical Brain Region
J. Neurosci.,
February 11, 2004;
24(6):
1478 - 1485.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|