 |
Previous Article | Next Article 
The Journal of Neuroscience, April 15, 2001, 21(8):2793-2798
Predictability Modulates Human Brain Response to Reward
Gregory S.
Berns1,
Samuel M.
McClure2,
Giuseppe
Pagnoni1, and
P.
Read
Montague2
1 Department of Psychiatry and Behavioral Sciences,
Emory University School of Medicine, Atlanta, Georgia 30322, and
2 Center for Theoretical Neuroscience, Division of
Neuroscience, Baylor College of Medicine, Houston, Texas 77030
Certain classes of stimuli, such as food and drugs, are highly
effective in activating reward regions. We show in humans that activity
in these regions can be modulated by the predictability of the
sequenced delivery of two mildly pleasurable stimuli, orally delivered fruit juice and water. Using functional magnetic resonance imaging, the activity for rewarding stimuli in both the nucleus accumbens and medial orbitofrontal cortex was greatest when the stimuli
were unpredictable. Moreover, the subjects' stated preference for
either juice or water was not directly correlated with activity in
reward regions but instead was correlated with activity in sensorimotor
cortex. For pleasurable stimuli, these findings suggest that
predictability modulates the response of human reward regions, and
subjective preference can be dissociated from this response.
Key words:
reward; dopamine; fMRI; reinforcement; neural network; nucleus accumbens; striatum
Copyright © 2001 Society for Neuroscience 0270-6474/01/2182793-06$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
D. Talmi, P. Dayan, S. J. Kiebel, C. D. Frith, and R. J. Dolan
How Humans Integrate the Prospects of Pain and Reward during Choice
J. Neurosci.,
November 18, 2009;
29(46):
14617 - 14626.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. L. Glocker, D. D. Langleben, K. Ruparel, J. W. Loughead, J. N. Valdez, M. D. Griffin, N. Sachser, and R. C. Gur
Baby schema modulates the brain reward system in nulliparous women
PNAS,
June 2, 2009;
106(22):
9115 - 9119.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. A. Pizzagalli, A. J. Holmes, D. G. Dillon, E. L. Goetz, J. L. Birk, R. Bogdan, D. D. Dougherty, D. V. Iosifescu, S. L. Rauch, and M. Fava
Reduced Caudate and Nucleus Accumbens Response to Rewards in Unmedicated Individuals With Major Depressive Disorder
Am J Psychiatry,
June 1, 2009;
166(6):
702 - 710.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. F. Rodriguez
Stimulus-outcome learnability differentially activates anterior cingulate and hippocampus at feedback processing
Learn. Mem.,
April 29, 2009;
16(5):
324 - 331.
[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,
February 1, 2009;
19(2):
284 - 292.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. H. Zald, R. L. Cowan, P. Riccardi, R. M. Baldwin, M. S. Ansari, R. Li, E. S. Shelby, C. E. Smith, M. McHugo, and R. M. Kessler
Midbrain Dopamine Receptor Availability Is Inversely Associated with Novelty-Seeking Traits in Humans
J. Neurosci.,
December 31, 2008;
28(53):
14372 - 14378.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. M. COX, H. J. AIZENSTEIN, and J. A. FIEZ
Striatal outcome processing in healthy aging
Cogn Affect Behav Neurosci,
September 1, 2008;
8(3):
304 - 317.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
N. J. Diederich and C. G. Goetz
The placebo treatments in neurosciences: New insights from clinical and neuroimaging studies
Neurology,
August 26, 2008;
71(9):
677 - 684.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. M. Gilman, V. A. Ramchandani, M. B. Davis, J. M. Bjork, and D. W. Hommer
Why We Like to Drink: A Functional Magnetic Resonance Imaging Study of the Rewarding and Anxiolytic Effects of Alcohol
J. Neurosci.,
April 30, 2008;
28(18):
4583 - 4591.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Van Duynslaeger, F. Van Overwalle, and E. Verstraeten
Electrophysiological time course and brain areas of spontaneous and intentional trait inferences
Soc Cogn Affect Neurosci,
September 1, 2007;
2(3):
174 - 188.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. M. Williams and E. Gordon
Dynamic Organization of the Emotional Brain: Responsivity, Stability, and Instability
Neuroscientist,
August 1, 2007;
13(4):
349 - 370.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
M. G. Veldhuizen, G. Bender, R. T. Constable, and D. M. Small
Trying to Detect Taste in a Tasteless Solution: Modulation of Early Gustatory Cortex by Attention to Taste
Chem Senses,
July 1, 2007;
32(6):
569 - 581.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Hasler, S. Fromm, R. P. Alvarez, D. A. Luckenbaugh, W. C. Drevets, and C. Grillon
Cerebral Blood Flow in Immediate and Sustained Anxiety
J. Neurosci.,
June 6, 2007;
27(23):
6313 - 6319.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. M. McClure, K. M. Ericson, D. I. Laibson, G. Loewenstein, and J. D. Cohen
Time Discounting for Primary Rewards
J. Neurosci.,
May 23, 2007;
27(21):
5796 - 5804.
[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]
|
 |
|

|
 |

|
 |
 
J. J. Day and R. M. Carelli
The Nucleus Accumbens and Pavlovian Reward Learning
Neuroscientist,
April 1, 2007;
13(2):
148 - 159.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Landmann, S. Dehaene, S. Pappata, A. Jobert, M. Bottlaender, D. Roumenov, and D. Le Bihan
Dynamics of Prefrontal and Cingulate Activity during a Reward-Based Logical Deduction Task
Cereb Cortex,
April 1, 2007;
17(4):
749 - 759.
[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]
|
 |
|

|
 |

|
 |
 
P. W. Kalivas and N. D. Volkow
The Neural Basis of Addiction: A Pathology of Motivation and Choice
Focus,
January 1, 2007;
5(2):
208 - 219.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Pecina, K. S. Smith, and K. C. Berridge
Hedonic Hot Spots in the Brain
Neuroscientist,
December 1, 2006;
12(6):
500 - 511.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
R. B. Postuma and A. Dagher
Basal Ganglia Functional Connectivity Based on a Meta-Analysis of 126 Positron Emission Tomography and Functional Magnetic Resonance Imaging Publications
Cereb Cortex,
October 1, 2006;
16(10):
1508 - 1521.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Yacubian, J. Glascher, K. Schroeder, T. Sommer, D. F. Braus, and C. Buchel
Dissociable systems for gain- and loss-related value predictions and errors of prediction in the human brain.
J. Neurosci.,
September 13, 2006;
26(37):
9530 - 9537.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. E. Guyer, E. E. Nelson, K. Perez-Edgar, M. G. Hardin, R. Roberson-Nay, C. S. Monk, J. M. Bjork, H. A. Henderson, D. S. Pine, N. A. Fox, et al.
Striatal functional alteration in adolescents characterized by early childhood behavioral inhibition.
J. Neurosci.,
June 14, 2006;
26(24):
6399 - 6405.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. F. Taylor, B. Martis, K. D. Fitzgerald, R. C. Welsh, J. L. Abelson, I. Liberzon, J. A. Himle, and W. J. Gehring
Medial Frontal Cortex Activity and Loss-Related Responses to Errors
J. Neurosci.,
April 12, 2006;
26(15):
4063 - 4070.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-C. Dreher, P. Kohn, and K. F. Berman
Neural Coding of Distinct Statistical Properties of Reward Information in Humans
Cereb Cortex,
April 1, 2006;
16(4):
561 - 573.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Haruno and M. Kawato
Different Neural Correlates of Reward Expectation and Reward Expectation Error in the Putamen and Caudate Nucleus During Stimulus-Action-Reward Association Learning
J Neurophysiol,
February 1, 2006;
95(2):
948 - 959.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Galvan, T. A. Hare, M. Davidson, J. Spicer, G. Glover, and B. J. Casey
The Role of Ventral Frontostriatal Circuitry in Reward-Based Learning in Humans
J. Neurosci.,
September 21, 2005;
25(38):
8650 - 8656.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. W. Kalivas and N. D. Volkow
The Neural Basis of Addiction: A Pathology of Motivation and Choice
Am J Psychiatry,
August 1, 2005;
162(8):
1403 - 1413.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Aron, H. Fisher, D. J. Mashek, G. Strong, H. Li, and L. L. Brown
Reward, Motivation, and Emotion Systems Associated With Early-Stage Intense Romantic Love
J Neurophysiol,
July 1, 2005;
94(1):
327 - 337.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. D. Volkow, G.-J. Wang, Y. Ma, J. S. Fowler, C. Wong, Y.-S. Ding, R. Hitzemann, J. M. Swanson, and P. Kalivas
Activation of Orbital and Medial Prefrontal Cortex by Methylphenidate in Cocaine-Addicted Subjects But Not in Controls: Relevance to Addiction
J. Neurosci.,
April 13, 2005;
25(15):
3932 - 3939.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Seger and C. M. Cincotta
The Roles of the Caudate Nucleus in Human Classification Learning
J. Neurosci.,
March 16, 2005;
25(11):
2941 - 2951.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Winkielman, K. C. Berridge, and J. L. Wilbarger
Unconscious Affective Reactions to Masked Happy Versus Angry Faces Influence Consumption Behavior and Judgments of Value
Pers Soc Psychol Bull,
January 1, 2005;
31(1):
121 - 135.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Sotres-Bayon, D. E.A. Bush, and J. E. LeDoux
Emotional Perseveration: An Update on Prefrontal-Amygdala Interactions in Fear Extinction
Learn. Mem.,
September 1, 2004;
11(5):
525 - 535.
[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]
|
 |
|

|
 |

|
 |
 
A. R. Aron, D. Shohamy, J. Clark, C. Myers, M. A. Gluck, and R. A. Poldrack
Human Midbrain Sensitivity to Cognitive Feedback and Uncertainty During Classification Learning
J Neurophysiol,
August 1, 2004;
92(2):
1144 - 1152.
[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]
|
 |
|

|
 |

|
 |
 
M. Haruno, T. Kuroda, K. Doya, K. Toyama, M. Kimura, K. Samejima, H. Imamizu, and M. Kawato
A Neural Correlate of Reward-Based Behavioral Learning in Caudate Nucleus: A Functional Magnetic Resonance Imaging Study of a Stochastic Decision Task
J. Neurosci.,
February 18, 2004;
24(7):
1660 - 1665.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. D. Kilts, R. E. Gross, T. D. Ely, and K. P.G. Drexler
The Neural Correlates of Cue-Induced Craving in Cocaine-Dependent Women
Am J Psychiatry,
February 1, 2004;
161(2):
233 - 241.
[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. 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]
|
 |
|

|
 |

|
 |
 
M. Ullsperger and D. Y. von Cramon
Error Monitoring Using External Feedback: Specific Roles of the Habenular Complex, the Reward System, and the Cingulate Motor Area Revealed by Functional Magnetic Resonance Imaging
J. Neurosci.,
May 15, 2003;
23(10):
4308 - 4314.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E.T. Rolls, J. O'Doherty, M.L. Kringelbach, S. Francis, R. Bowtell, and F. McGlone
Representations of Pleasant and Painful Touch in the Human Orbitofrontal and Cingulate Cortices
Cereb Cortex,
March 1, 2003;
13(3):
308 - 317.
[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]
|
 |
|

|
 |

|
 |
 
G. Bush, B. A. Vogt, J. Holmes, A. M. Dale, D. Greve, M. A. Jenike, and B. R. Rosen
Dorsal anterior cingulate cortex: A role in reward-based decision making
PNAS,
December 21, 2001;
(2001)
12470999.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Bush, B. A. Vogt, J. Holmes, A. M. Dale, D. Greve, M. A. Jenike, and B. R. Rosen
Dorsal anterior cingulate cortex: A role in reward-based decision making
PNAS,
January 8, 2002;
99(1):
523 - 528.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Knutson, C. M. Adams, G. W. Fong, and D. Hommer
Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens
J. Neurosci.,
August 15, 2001;
21(16):
RC159 - RC159.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|