Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Science 22 August 2003:
Vol. 301. no. 5636, pp. 1104 - 1107
DOI: 10.1126/science.1087919

Reports

Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex

Jay A. Gottfried,* John O'Doherty, Raymond J. Dolan

Adaptive behavior is optimized in organisms that maintain flexible representations of the value of sensory-predictive cues. To identify central representations of predictive reward value in humans, we used reinforcer devaluation while measuring neural activity with functional magnetic resonance imaging. We presented two arbitrary visual stimuli, both before and after olfactory devaluation, in a paradigm of appetitive conditioning. In amygdala and orbitofrontal cortex, responses evoked by a predictive target stimulus were decreased after devaluation, whereas responses to the nondevalued stimulus were maintained. Thus, differential activity in amygdala and orbitofrontal cortex encodes the current value of reward representations accessible to predictive cues.

Functional Imaging Laboratory, Wellcome Department of Imaging Neuroscience, 12 Queen Square, London WC1N 3BG, UK.

* To whom correspondence should be addressed. E-mail: j.gottfried{at}fil.ion.ucl.ac.uk

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Rating a New Hedonic Scale: A Commentary on "Derivation and Evaluation of a Labeled Hedonic Scale" by Lim, Wood and Green.
J. Prescott (2009)
Chem Senses 34, 735-737
   Full Text »    PDF »
Ventral Striatal Neurons Encode the Value of the Chosen Action in Rats Deciding between Differently Delayed or Sized Rewards.
M. R. Roesch, T. Singh, P. L. Brown, S. E. Mullins, and G. Schoenbaum (2009)
J. Neurosci. 29, 13365-13376
   Abstract »    Full Text »    PDF »
Neural computations underlying action-based decision making in the human brain.
K. Wunderlich, A. Rangel, and J. P. O'Doherty (2009)
PNAS 106, 17199-17204
   Abstract »    Full Text »    PDF »
The amygdala is not necessary for unconditioned stimulus inflation after Pavlovian fear conditioning in rats.
C. A. Rabinak, C. A. Orsini, J. M. Zimmerman, and S. Maren (2009)
Learn. Mem. 16, 645-654
   Abstract »    Full Text »    PDF »
Neural responses to sanction threats in two-party economic exchange.
J. Li, E. Xiao, D. Houser, and P. R. Montague (2009)
PNAS 106, 16835-16840
   Abstract »    Full Text »    PDF »
The Neural Basis of Categorical Face Perception: Graded Representations of Face Gender in Fusiform and Orbitofrontal Cortices.
J. B. Freeman, N. O. Rule, R. B. Adams Jr, and N. Ambady (2009)
Cereb Cortex
   Abstract »    Full Text »    PDF »
The Convergence of Information about Rewarding and Aversive Stimuli in Single Neurons.
S. E. Morrison and C. D. Salzman (2009)
J. Neurosci. 29, 11471-11483
   Abstract »    Full Text »    PDF »
Differential Engagement of the Ventromedial Prefrontal Cortex by Goal-Directed and Habitual Behavior toward Food Pictures in Humans.
S. de Wit, P. R. Corlett, M. R. Aitken, A. Dickinson, and P. C. Fletcher (2009)
J. Neurosci. 29, 11330-11338
   Abstract »    Full Text »    PDF »
Right Ventromedial and Dorsolateral Prefrontal Cortices Mediate Adaptive Decisions under Ambiguity by Integrating Choice Utility and Outcome Evaluation.
A. Christakou, M. Brammer, V. Giampietro, and K. Rubia (2009)
J. Neurosci. 29, 11020-11028
   Abstract »    Full Text »    PDF »
The Role of Human Orbitofrontal Cortex in Value Comparison for Incommensurable Objects.
T. H. B. FitzGerald, B. Seymour, and R. J. Dolan (2009)
J. Neurosci. 29, 8388-8395
   Abstract »    Full Text »    PDF »
Toward a Model of Impaired Reality Testing in Rats.
M. McDannald and G. Schoenbaum (2009)
Schizophr Bull 35, 664-667
   Abstract »    Full Text »    PDF »
Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women.
K. N. Spreckelmeyer, S. Krach, G. Kohls, L. Rademacher, A. Irmak, K. Konrad, T. Kircher, and G. Grunder (2009)
Soc Cogn Affect Neurosci 4, 158-165
   Abstract »    Full Text »    PDF »
Rewarding Morphine-Induced Synaptic Function of {delta}-Opioid Receptors on Central Glutamate Synapses.
B. Bie, W. Zhu, and Z. Z. Pan (2009)
J. Pharmacol. Exp. Ther. 329, 290-296
   Abstract »    Full Text »    PDF »
Thinking like a trader selectively reduces individuals' loss aversion.
P. Sokol-Hessner, M. Hsu, N. G. Curley, M. R. Delgado, C. F. Camerer, and E. A. Phelps (2009)
PNAS 106, 5035-5040
   Abstract »    Full Text »    PDF »
How Choice Reveals and Shapes Expected Hedonic Outcome.
T. Sharot, B. De Martino, and R. J. Dolan (2009)
J. Neurosci. 29, 3760-3765
   Abstract »    Full Text »    PDF »
Short-Term Temporal Discounting of Reward Value in Human Ventral Striatum.
L. Gregorios-Pippas, P. N. Tobler, and W. Schultz (2009)
J Neurophysiol 101, 1507-1523
   Abstract »    Full Text »    PDF »
Evidence of gender differences in the ability to inhibit brain activation elicited by food stimulation.
G.-J. Wang, N. D. Volkow, F. Telang, M. Jayne, Y. Ma, K. Pradhan, W. Zhu, C. T. Wong, P. K. Thanos, A. Geliebter, et al. (2009)
PNAS 106, 1249-1254
   Abstract »    Full Text »    PDF »
Mesolimbic Functional Magnetic Resonance Imaging Activations during Reward Anticipation Correlate with Reward-Related Ventral Striatal Dopamine Release.
B. H. Schott, L. Minuzzi, R. M. Krebs, D. Elmenhorst, M. Lang, O. H. Winz, C. I. Seidenbecher, H. H. Coenen, H.-J. Heinze, K. Zilles, et al. (2008)
J. Neurosci. 28, 14311-14319
   Abstract »    Full Text »    PDF »
The role of the striatum in aversive learning and aversive prediction errors.
M. R Delgado, J. Li, D. Schiller, and E. A Phelps (2008)
Phil Trans R Soc B 363, 3787-3800
   Abstract »    Full Text »    PDF »
Conceptual representations in goal-directed decision making.
N. Shea, K. Krug, and P. N. Tobler (2008)
Cogn Affect Behav Neurosci 8, 418-428
   Abstract »    PDF »
A neural basis for the effect of candidate appearance on election outcomes.
M. L. Spezio, A. Rangel, R. M. Alvarez, J. P. O'Doherty, K. Mattes, A. Todorov, H. Kim, and R. Adolphs (2008)
Soc Cogn Affect Neurosci 3, 344-352
   Abstract »    Full Text »    PDF »
The Spatial Attention Network Interacts with Limbic and Monoaminergic Systems to Modulate Motivation-Induced Attention Shifts.
A. Mohanty, D. R. Gitelman, D. M. Small, and M. M. Mesulam (2008)
Cereb Cortex 18, 2604-2613
   Abstract »    Full Text »    PDF »
Relation Between Obesity and Blunted Striatal Response to Food Is Moderated by TaqIA A1 Allele.
E. Stice, S. Spoor, C. Bohon, and D. M. Small (2008)
Science 322, 449-452
   Abstract »    Full Text »    PDF »
Cortical regions activated by the subjective sense of perceptual coherence of environmental sounds: A proposal for a neuroscience of intuition.
K. G. VOLZ, R. RUBSAMEN, and D. Y. VON CRAMON (2008)
Cogn Affect Behav Neurosci 8, 318-328
   Abstract »    PDF »
Amygdala Volume Associated With Alcohol Abuse Relapse and Craving.
J. Wrase, N. Makris, D. F. Braus, K. Mann, M. N. Smolka, D. N. Kennedy, V. S. Caviness, S. M. Hodge, L. Tang, M. Albaugh, et al. (2008)
Am J Psychiatry 165, 1179-1184
   Abstract »    Full Text »    PDF »
Calculating Consequences: Brain Systems That Encode the Causal Effects of Actions.
S. C. Tanaka, B. W. Balleine, and J. P. O'Doherty (2008)
J. Neurosci. 28, 6750-6755
   Abstract »    Full Text »    PDF »
Abnormal Ventromedial Prefrontal Cortex Function in Children With Psychopathic Traits During Reversal Learning.
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. (2008)
Arch Gen Psychiatry 65, 586-594
   Abstract »    Full Text »    PDF »
Dynamic Changes in Representations of Preceding and Upcoming Reward in Monkey Orbitofrontal Cortex.
J. M. Simmons and B. J. Richmond (2008)
Cereb Cortex 18, 93-103
   Abstract »    Full Text »    PDF »
Orbitofrontal volume deficit in schizophrenia and thought disorder.
M. Nakamura, P. G. Nestor, J. J. Levitt, A. S. Cohen, T. Kawashima, M. E. Shenton, and R. W. McCarley (2008)
Brain 131, 180-195
   Abstract »    Full Text »    PDF »
Mindfulness training and neural integration: differentiation of distinct streams of awareness and the cultivation of well-being.
D. J. Siegel (2007)
Soc Cogn Affect Neurosci 2, 259-263
   Full Text »    PDF »
Effects of overfeeding on the neuronal response to visual food cues.
M.-A. Cornier, S. S Von Kaenel, D. H Bessesen, and J. R Tregellas (2007)
Am. J. Clinical Nutrition 86, 965-971
   Abstract »    Full Text »    PDF »
Control of appetitive and aversive taste-reactivity responses by an auditory conditioned stimulus in a devaluation task: A FOS and behavioral analysis.
E. C. Kerfoot, I. Agarwal, H. J. Lee, and P. C. Holland (2007)
Learn. Mem. 14, 581-589
   Abstract »    Full Text »    PDF »
Genetic modulation of cognitive flexibility and socioemotional behavior in rhesus monkeys.
A. Izquierdo, T. K. Newman, J. D. Higley, and E. A. Murray (2007)
PNAS 104, 14128-14133
   Abstract »    Full Text »    PDF »
What We Know and Do Not Know about the Functions of the Orbitofrontal Cortex after 20 Years of Cross-Species Studies.
E. A. Murray, J. P. O'Doherty, and G. Schoenbaum (2007)
J. Neurosci. 27, 8166-8169
   Abstract »    Full Text »    PDF »
Medial Prefrontal Cortex Is Necessary for an Appetitive Contextual Conditioned Stimulus to Promote Eating in Sated Rats.
G. D. Petrovich, C. A. Ross, P. C. Holland, and M. Gallagher (2007)
J. Neurosci. 27, 6436-6441
   Abstract »    Full Text »    PDF »
Associative Encoding in Posterior Piriform Cortex during Odor Discrimination and Reversal Learning.
D. J. Calu, M. R. Roesch, T. A. Stalnaker, and G. Schoenbaum (2007)
Cereb Cortex 17, 1342-1349
   Abstract »    Full Text »    PDF »
The human amygdala and orbital prefrontal cortex in behavioural regulation.
R.J Dolan (2007)
Phil Trans R Soc B 362, 787-799
   Abstract »    Full Text »    PDF »
Determining the Neural Substrates of Goal-Directed Learning in the Human Brain.
V. V. Valentin, A. Dickinson, and J. P. O'Doherty (2007)
J. Neurosci. 27, 4019-4026
   Abstract »    Full Text »    PDF »
Neural Coding of Reward-Prediction Error Signals During Classical Conditioning With Attractive Faces.
S. Bray and J. O'Doherty (2007)
J Neurophysiol 97, 3036-3045
   Abstract »    Full Text »    PDF »
Altered orbitofrontal sulcogyral pattern in schizophrenia.
M. Nakamura, P. G. Nestor, R. W. McCarley, J. J. Levitt, L. Hsu, T. Kawashima, M. Niznikiewicz, and M. E. Shenton (2007)
Brain 130, 693-707
   Abstract »    Full Text »    PDF »
Associative Encoding in Anterior Piriform Cortex versus Orbitofrontal Cortex during Odor Discrimination and Reversal Learning.
M. R. Roesch, T. A. Stalnaker, and G. Schoenbaum (2007)
Cereb Cortex 17, 643-652
   Abstract »    Full Text »    PDF »
Menstrual cycle phase modulates reward-related neural function in women.
J.-C. Dreher, P. J. Schmidt, P. Kohn, D. Furman, D. Rubinow, and K. F. Berman (2007)
PNAS 104, 2465-2470
   Abstract »    Full Text »    PDF »
Decoding the neural substrates of reward-related decision making with functional MRI.
A. N. Hampton and J. P. O'Doherty (2007)
PNAS 104, 1377-1382
   Abstract »    Full Text »    PDF »
Involvement of Non-NMDA Glutamate Receptors in Central Amygdala in Synaptic Actions of Ethanol and Ethanol-Induced Reward Behavior.
W. Zhu, B. Bie, and Z. Z. Pan (2007)
J. Neurosci. 27, 289-298
   Abstract »    Full Text »    PDF »
Amygdaloid lesion-induced obesity: relation to sexual behavior, olfaction, and the ventromedial hypothalamus.
B. M. King (2006)
Am J Physiol Regulatory Integrative Comp Physiol 291, R1201-R1214
   Abstract »    Full Text »    PDF »
The Role of the Ventromedial Prefrontal Cortex in Abstract State-Based Inference during Decision Making in Humans..
A. N. Hampton, P. Bossaerts, and J. P. O'Doherty (2006)
J. Neurosci. 26, 8360-8367
   Abstract »    Full Text »    PDF »
Individual differences in reward drive predict neural responses to images of food..
J. D. Beaver, A. D. Lawrence, J. van Ditzhuijzen, M. H. Davis, A. Woods, and A. J. Calder (2006)
J. Neurosci. 26, 5160-5166
   Abstract »    Full Text »    PDF »
Pictures of Appetizing Foods Activate Gustatory Cortices for Taste and Reward.
W. K. Simmons, A. Martin, and L. W. Barsalou (2005)
Cereb Cortex 15, 1602-1608
   Abstract »    Full Text »    PDF »
Quantitative Investigation of Connections of the Prefrontal Cortex in the Human and Macaque using Probabilistic Diffusion Tractography.
P. L. Croxson, H. Johansen-Berg, T. E. J. Behrens, M. D. Robson, M. A. Pinsk, C. G. Gross, W. Richter, M. C. Richter, S. Kastner, and M. F. S. Rushworth (2005)
J. Neurosci. 25, 8854-8866
   Abstract »    Full Text »    PDF »
Integrated Neural Representations of Odor Intensity and Affective Valence in Human Amygdala.
J. S. Winston, J. A. Gottfried, J. M. Kilner, and R. J. Dolan (2005)
J. Neurosci. 25, 8903-8907
   Abstract »    Full Text »    PDF »
Amygdalar and Prefrontal Pathways to the Lateral Hypothalamus Are Activated by a Learned Cue That Stimulates Eating.
G. D. Petrovich, P. C. Holland, and M. Gallagher (2005)
J. Neurosci. 25, 8295-8302
   Abstract »    Full Text »    PDF »
Sex Differences in the Responses of the Human Amygdala.
S. Hamann (2005)
Neuroscientist 11, 288-293
   Abstract »    PDF »
Neurobiology of Mice Selected for High Voluntary Wheel-running Activity.
J. S. Rhodes, S. C. Gammie, and T. Garland Jr. (2005)
Integr. Comp. Biol. 45, 438-455
   Abstract »    Full Text »    PDF »
Color of Scents: Chromatic Stimuli Modulate Odor Responses in the Human Brain.
R. A. Osterbauer, P. M. Matthews, M. Jenkinson, C. F. Beckmann, P. C. Hansen, and G. A. Calvert (2005)
J Neurophysiol 93, 3434-3441
   Abstract »    Full Text »    PDF »
GABAA-Mediated Inhibition of Basolateral Amygdala Blocks Reward Devaluation in Macaques.
L. L. Wellman, K. Gale, and L. Malkova (2005)
J. Neurosci. 25, 4577-4586
   Abstract »    Full Text »    PDF »
Double Dissociation of Exteroceptive and Interoceptive Feedback Systems in the Orbital and Ventromedial Prefrontal Cortex of Humans.
E. Hurliman, J. C. Nagode, and J. V. Pardo (2005)
J. Neurosci. 25, 4641-4648
   Abstract »    Full Text »    PDF »
Learning to Like: A Role for Human Orbitofrontal Cortex in Conditioned Reward.
S. M. L. Cox, A. Andrade, and I. S. Johnsrude (2005)
J. Neurosci. 25, 2733-2740
   Abstract »    Full Text »    PDF »
Opposite Effects of Amphetamine Self-administration Experience on Dendritic Spines in the Medial and Orbital Prefrontal Cortex.
H. S. Crombag, G. Gorny, Y. Li, B. Kolb, and T. E. Robinson (2005)
Cereb Cortex 15, 341-348
   Abstract »    Full Text »    PDF »
Consolidation and Reconsolidation of Incentive Learning in the Amygdala.
S.-H. Wang, S. B. Ostlund, K. Nader, and B. W. Balleine (2005)
J. Neurosci. 25, 830-835
   Abstract »    Full Text »    PDF »
The Cognitive Neuroscience of Human Decision Making: A Review and Conceptual Framework.
L. K. Fellows (2004)
Behav Cogn Neurosci Rev 3, 159-172
   Abstract »    PDF »
Bilateral Orbital Prefrontal Cortex Lesions in Rhesus Monkeys Disrupt Choices Guided by Both Reward Value and Reward Contingency.
A. Izquierdo, R. K. Suda, and E. A. Murray (2004)
J. Neurosci. 24, 7540-7548
   Abstract »    Full Text »    PDF »
Differential Involvement of Orbitofrontal Cortex Subregions in Conditioned Cue-Induced and Cocaine-Primed Reinstatement of Cocaine Seeking in Rats.
R. A. Fuchs, K. A. Evans, M. P. Parker, and R. E. See (2004)
J. Neurosci. 24, 6600-6610
   Abstract »    Full Text »    PDF »
The Amygdala Is Enlarged in Children But Not Adolescents with Autism; the Hippocampus Is Enlarged at All Ages.
C. M. Schumann, J. Hamstra, B. L. Goodlin-Jones, L. J. Lotspeich, H. Kwon, M. H. Buonocore, C. R. Lammers, A. L. Reiss, and D. G. Amaral (2004)
J. Neurosci. 24, 6392-6401
   Abstract »    Full Text »    PDF »
Distinctive Responses in the Medial Amygdala to Same-Species and Different-Species Pheromones.
M. Meredith and J. M. Westberry (2004)
J. Neurosci. 24, 5719-5725
   Abstract »    Full Text »    PDF »
The Neural Substrates of Reward Processing in Humans: The Modern Role of fMRI.
S. M. McClure, M. K. York, and P. R. Montague (2004)
Neuroscientist 10, 260-268
   Abstract »    PDF »
Combined Unilateral Lesions of the Amygdala and Orbital Prefrontal Cortex Impair Affective Processing in Rhesus Monkeys.
A. Izquierdo and E. A. Murray (2004)
J Neurophysiol 91, 2023-2039
   Abstract »    Full Text »    PDF »
The human cortex responds to an interoceptive challenge.
H. D. Critchley (2004)
PNAS 101, 6333-6334
   Full Text »    PDF »



To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)