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J Neurophysiol 80: 1-27, 1998;
0022-3077/98 $5.00
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The Journal of Neurophysiology Vol. 80 No. 1 July 1998, pp. 1-27
Copyright ©1998 The American Physiological Society

INVITED REVIEW


Predictive Reward Signal of Dopamine Neurons

Wolfram Schultz

Institute of Physiology and Program in Neuroscience, University of Fribourg, CH-1700 Fribourg, Switzerland

Schultz, Wolfram. Predictive reward signal of dopamine neurons. J. Neurophysiol. 80: 1-27, 1998. The effects of lesions, receptor blocking, electrical self-stimulation, and drugs of abuse suggest that midbrain dopamine systems are involved in processing reward information and learning approach behavior. Most dopamine neurons show phasic activations after primary liquid and food rewards and conditioned, reward-predicting visual and auditory stimuli. They show biphasic, activation-depression responses after stimuli that resemble reward-predicting stimuli or are novel or particularly salient. However, only few phasic activations follow aversive stimuli. Thus dopamine neurons label environmental stimuli with appetitive value, predict and detect rewards and signal alerting and motivating events. By failing to discriminate between different rewards, dopamine neurons appear to emit an alerting message about the surprising presence or absence of rewards. All responses to rewards and reward-predicting stimuli depend on event predictability. Dopamine neurons are activated by rewarding events that are better than predicted, remain uninfluenced by events that are as good as predicted, and are depressed by events that are worse than predicted. By signaling rewards according to a prediction error, dopamine responses have the formal characteristics of a teaching signal postulated by reinforcement learning theories. Dopamine responses transfer during learning from primary rewards to reward-predicting stimuli. This may contribute to neuronal mechanisms underlying the retrograde action of rewards, one of the main puzzles in reinforcement learning. The impulse response releases a short pulse of dopamine onto many dendrites, thus broadcasting a rather global reinforcement signal to postsynaptic neurons. This signal may improve approach behavior by providing advance reward information before the behavior occurs, and may contribute to learning by modifying synaptic transmission. The dopamine reward signal is supplemented by activity in neurons in striatum, frontal cortex, and amygdala, which process specific reward information but do not emit a global reward prediction error signal. A cooperation between the different reward signals may assure the use of specific rewards for selectively reinforcing behaviors. Among the other projection systems, noradrenaline neurons predominantly serve attentional mechanisms and nucleus basalis neurons code rewards heterogeneously. Cerebellar climbing fibers signal errors in motor performance or errors in the prediction of aversive events to cerebellar Purkinje cells. Most deficits following dopamine-depleting lesions are not easily explained by a defective reward signal but may reflect the absence of a general enabling function of tonic levels of extracellular dopamine. Thus dopamine systems may have two functions, the phasic transmission of reward information and the tonic enabling of postsynaptic neurons.




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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]

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 J. Neurosci.Home page
G. Cui, B. E. Bernier, M. T. Harnett, and H. Morikawa
Differential Regulation of Action Potential- and Metabotropic Glutamate Receptor-Induced Ca2+ Signals by Inositol 1,4,5-Trisphosphate in Dopaminergic Neurons
J. Neurosci., April 25, 2007; 27(17): 4776 - 4785.
[Abstract] [Full Text] [PDF]

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 Pers Soc Psychol BullHome page
L. D. Smillie, L. I. Dalgleish, and C. J. Jackson
Distinguishing Between Learning and Motivation in Behavioral Tests of the Reinforcement Sensitivity Theory of Personality
Pers Soc Psychol Bull, April 1, 2007; 33(4): 476 - 489.
[Abstract] [PDF]

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 Adaptive BehaviorHome page
M. Witkowski
An Action-Selection Calculus
Adaptive Behavior, March 1, 2007; 15(1): 73 - 97.
[Abstract] [PDF]

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 Soc Cogn Affect NeurosciHome page
M. X Cohen
Individual differences and the neural representations of reward expectation and reward prediction error
Soc Cogn Affect Neurosci, March 1, 2007; 2(1): 20 - 30.
[Abstract] [Full Text] [PDF]

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 J. Neurophysiol.Home page
P. W. German and H. L. Fields
Rat Nucleus Accumbens Neurons Persistently Encode Locations Associated With Morphine Reward
J Neurophysiol, March 1, 2007; 97(3): 2094 - 2106.
[Abstract] [Full Text] [PDF]

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 Arch Gen PsychiatryHome page
B. W. Dunlop and C. B. Nemeroff
The Role of Dopamine in the Pathophysiology of Depression
Arch Gen Psychiatry, March 1, 2007; 64(3): 327 - 337.
[Full Text] [PDF]

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 J. Neurosci.Home page
S. B. Floresco and M. T. Tse
Dopaminergic Regulation of Inhibitory and Excitatory Transmission in the Basolateral Amygdala-Prefrontal Cortical Pathway
J. Neurosci., February 21, 2007; 27(8): 2045 - 2057.
[Abstract] [Full Text] [PDF]

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 FocusHome page
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]

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 FocusHome page
S. E. Hyman
Addiction: A Disease of Learning and Memory
Focus, January 1, 2007; 5(2): 220 - 228.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
E. B. Margolis, H. Lock, G. O. Hjelmstad, and H. L. Fields
The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons?
J. Physiol., December 15, 2006; 577(3): 907 - 924.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
M. D. Humphries, R. D. Stewart, and K. N. Gurney
A Physiologically Plausible Model of Action Selection and Oscillatory Activity in the Basal Ganglia
J. Neurosci., December 13, 2006; 26(50): 12921 - 12942.
[Abstract] [Full Text] [PDF]

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 NeuroscientistHome page
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]


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