Dopamine signals for reward value and risk: basic and recent data
Open accessAbstract
BACKGROUND: Previous lesion, electrical self-stimulation and drug addiction studies suggest that the midbrain dopamine systems are parts of the reward system of the brain. This review provides an updated overview about the basic signals of dopamine neurons to environmental stimuli. METHODS: The described experiments used standard behavioral and neurophysiological methods to record the activity of single dopamine neurons in awake monkeys during specific behavioral tasks. RESULTS: Dopamine neurons show phasic activations to external stimuli. The signal reflects reward, physical salience, risk and punishment, in descending order of fractions of responding neurons. Expected reward value is a key decision variable for economic choices. The reward response codes reward value, probability and their summed product, expected value. The neurons code reward value as it differs from prediction, thus fulfilling the basic requirement for a bidirectional prediction error teaching signal postulated by learning theory. This response is scaled in units of standard deviation. By contrast, relatively few dopamine neurons show the phasic activation following punishers and conditioned aversive stimuli, suggesting a lack of relationship of the reward response to general attention and arousal. Large proportions of dopamine neurons are also activated by intense, physically salient stimuli. This response is enhanced when the stimuli are novel; it appears to be distinct from the reward value signal. Dopamine neurons show also unspecific activations to non-rewarding stimuli that are possibly due to generalization by similar stimuli and pseudoconditioning by primary rewards. These activations are shorter than reward responses and are often followed by depression of activity. A separate, slower dopamine signal informs about risk, another important decision variable. The prediction error response occurs only with reward; it is scaled by the risk of predicted reward. CONCLUSIONS: Neurophysiological studies reveal phasic dopamine signals that transmit information related predominantly but not exclusively to reward. Although not being entirely homogeneous, the dopamine signal is more restricted and stereotyped than neuronal activity in most other brain structures involved in goal directed behavior.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The role of dopaminergic neurotransmission in the response to unpredicted or alerting sensory events is less well characterized.
“Less well characterized is the role of dopaminergic neurotransmission in the response to unpredicted or alerting sensory events, which may encourage investigation or prime motivated behavioral responses to these stimuli (Horvitz, 2000; Bromberg-Martin et al., 2010a; Schultz, 2010).”
From Ventral striatum dopamine release encodes unique properties of visual stimuli in mice (2023) · cites this paper as Schultz, 2010
While expectation of reward has received particular attention as a trigger for a dopamine response, other related cognitive-affective states are supported as well.
“While the expectation of reward has received particular attention as a trigger for a dopamine response (Schultz, 2013), other related cognitive-affective states are supported as well (Schultz, 2010).”
From Optimizing performance through intrinsic motivation and attention for learning: The OPTIMAL theory of motor learning (2016) · cites this paper as Schultz, 2010
Occasional risks to expected rewards (challenge) can transiently dampen extant levels of reward-related dopamine but amplify the impact of subsequent positive (but not negative) cues, strengthening the learning effect.
“Occasional risks to expected rewards (i.e., challenge) can transiently dampen the extant levels of rewardrelated dopamine but amplify the impact of subsequent Fig. 3 Schematic of the OPTIMAL theory positive (but not negative) cues, strengthening the learning effect (Schultz, 2010(Schultz, , 2013)).”
From Optimizing performance through intrinsic motivation and attention for learning: The OPTIMAL theory of motor learning (2016) · cites this paper as Schultz, 2010
The DAergic system, particularly the mesocorticolimbic pathway, is involved in drug addiction because DA modulates limbic and cortical sites for goal-directed behavior.
“The role of the DAergic system (in particular the mesocorticolimbic pathway) in drug addiction derives from DA’s ability to modulate many of the limbic and cortical sites involved in goal-directed behavior (Fig. 1) [18, 28–31].”
From Mechanistic insights into nicotine withdrawal (2011) · cites this paper as [31]
Once conditioning has occurred, DA signals act as a predictor of reward, incentivizing the animal to perform the behaviour that will result in consuming the expected reward.
“once conditioning has occurred, DA signals act as a predictor of reward (49), incentivizing the animal to perform the behaviour that will result in consuming the expected reward (drug or food).”
From Obesity and addiction: Neurobiological overlaps (2013) · cites this paper as [49]
DA signaling appears to code for a reward prediction error.
“This transition is conveyed through DA signaling, which appears to code for a 'reward prediction error' (Schultz 2010).”
From Food and Drug Reward: Overlapping Circuits in Human Obesity and Addiction (2011) · cites this paper as Schultz 2010
Some of these brain regions also serve to focus attention and promote DA-dependent attention and decision-making.
“In addition to mediating DA-related anxiety and habitual behaviour and learning (21,22), some of these brain regions also serve to focus attention and promote DA-dependent attention and decision-making (23).”
From Neuroendocrinology of Parental Response to Baby‐Cry (2011) · cites this paper as [23]
Decisions are assumed to track increased expected value, and social reward can influence value calculations.
“From a reward-learning perspective, decisions are assumed to track increased expected value (Niv & Montague, 2008; Schultz, 2010) and social reward can influence value calculations (Evans et al., 2011; Fehr, 2009).”
From Risk-taking and social exclusion in adolescence: neural mechanisms underlying peer influences on decision-making (2013) · cites this paper as Schultz, 2010
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · see citing works
Self-citationRescorla, R. A. (1972) · Medical Entomology and Zoology · Cited by 7,268 · see citing works
Rao, R. P. N., & Ballard, D. H. (1999) · Nature Neuroscience · doi:10.1038/4580 · Cited by 5,483 · cited 1× · see citing works
“Keeping up with the changing environmental situation by higher brain centers would simply involve updating the predictions with the less information containing, and less energy consuming, prediction errors rather than processing the full peripheral information every time one little thing has changed [4].”
BackgroundPredictive reward signal of dopamine neurons
Schultz, W. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.1.1 · Cited by 4,564 · see citing works
Self-citationClassical conditioning II: Current research and theory.
Black, A. H., & Prokasy, W. F. (1972) · Appleton-Century-Crofts eBooks · Cited by 4,449 · see citing works
Neural systems of reinforcement for drug addiction: from actions to habits to compulsion
Everitt, B. J., & Robbins, T. W. (2005) · Nature Neuroscience · doi:10.1038/nn1579 · Cited by 3,785 · see citing works
Pearce, J. M., & Hall, G. (1980) · Psychological Review · doi:10.1037/0033-295x.87.6.532 · Cited by 3,023 · see citing works
Exposition of a New Theory on the Measurement of Risk
Bernoulli, D. (1954) · Econometrica · doi:10.2307/1909829 · Cited by 2,779 · see citing works
A theory of attention: Variations in the associability of stimuli with reinforcement
Mackintosh, N. J. (1975) · Psychological Review · doi:10.1037/h0076778 · Cited by 2,733 · see citing works
Specious reward: A behavioral theory of impulsiveness and impulse control.
Ainslie, G. (1975) · Psychological Bulletin · doi:10.1037/h0076860 · Cited by 2,708 · see citing works
Discrete coding of reward probability and uncertainty by dopamine neurons
Fiorillo, C. D., Tobler, P. N., & Schultz, W. (2003) · Science · doi:10.1126/science.1077349 · Cited by 2,085 · see citing works
Self-citationA framework for mesencephalic dopamine systems based on predictive Hebbian learning
Montague, P., Dayan, P., & Sejnowski, T. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01936.1996 · Cited by 2,066 · see citing works
Wise, R. A., & Rompre, P.-P. (1989) · Annual Review of Psychology · doi:10.1146/annurev.ps.40.020189.001203 · Cited by 1,968 · see citing works
Toward a modern theory of adaptive networks: Expectation and prediction.
Sutton, R. S., & Barto, A. G. (1981) · Psychological Review · doi:10.1037/0033-295x.88.2.135 · Cited by 1,450 · see citing works
Multiple dopamine functions at different time courses
Schultz, W. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135722 · Cited by 1,415 · see citing works
Self-citationSynaptic plasticity and addiction
Kauer, J. A., & Malenka, R. C. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2234 · Cited by 1,397 · see citing works
Two types of dopamine neuron distinctly convey positive and negative motivational signals
Matsumoto, M., & Hikosaka, O. (2009) · Nature · doi:10.1038/nature08028 · Cited by 1,378 · see citing works
Midbrain dopamine neurons encode a quantitative reward prediction error signal
Bayer, H. M., & Glimcher, P. W. (2005) · Neuron · doi:10.1016/j.neuron.2005.05.020 · Cited by 1,304 · see citing works
Schultz, W., Apicella, P., & Ljungberg, T. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-03-00900.1993 · Cited by 1,291 · see citing works
Self-citationAdaptive Coding of Reward Value by Dopamine Neurons
Tobler, P. N., Fiorillo, C. D., & Schultz, W. (2005) · Science · doi:10.1126/science.1105370 · Cited by 1,276 · see citing works
Self-citationPhasic Firing in Dopaminergic Neurons Is Sufficient for Behavioral Conditioning
Tsai, H.-C., Zhang, F., Adamantidis, A., Stuber, G. D., Bonci, A., de Lecea, L., & Deisseroth, K. (2009) · Science · doi:10.1126/science.1168878 · Cited by 1,266 · see citing works
Dopamine neurons report an error in the temporal prediction of reward during learning
Hollerman, J. R., & Schultz, W. (1998) · Nature Neuroscience · doi:10.1038/1124 · Cited by 1,103 · see citing works
Self-citationDopamine responses comply with basic assumptions of formal learning theory
Waelti, P., Dickinson, A., & Schultz, W. (2001) · Nature · doi:10.1038/35083500 · Cited by 1,018 · see citing works
Self-citationResponses of monkey dopamine neurons during learning of behavioral reactions
Ljungberg, T., Apicella, P., & Schultz, W. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.1.145 · Cited by 987 · see citing works
Self-citationApproximating Expected Utility by a Function of Mean and Variance
Levy, H., & Markowtiz, H. M. (1979) · American Economic Review · Cited by 893 · see citing works
Pavlovian conditioned inhibition
Rescorla, R. (1969) · Psychological Bulletin · doi:10.1037/h0027760 · Cited by 868 · see citing works
Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli
Mirenowicz, J., & Schultz, W. (1996) · Nature · doi:10.1038/379449a0 · Cited by 829 · see citing works
Self-citationPhasic excitation of dopamine neurons in ventral VTA by noxious stimuli
Brischoux, F., Chakraborty, S., Brierley, D. I., & Ungless, M. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811507106 · Cited by 801 · see citing works
Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens
Day, J. J., Roitman, M. F., Wightman, R. M., & Carelli, R. M. (2007) · Nature Neuroscience · doi:10.1038/nn1923 · Cited by 710 · see citing works
Roesch, M. R., Calu, D. J., & Schoenbaum, G. (2007) · Nature Neuroscience · doi:10.1038/nn2013 · Cited by 597 · see citing works
Coincident but Distinct Messages of Midbrain Dopamine and Striatal Tonically Active Neurons
Morris, G., Arkadir, D., Nevet, A., Vaadia, E., & Bergman, H. (2004) · Neuron · doi:10.1016/j.neuron.2004.06.012 · Cited by 574 · see citing works
Midbrain dopamine neurons encode decisions for future action
Morris, G., Nevet, A., Arkadir, D., Vaadia, E., & Bergman, H. (2006) · Nature Neuroscience · doi:10.1038/nn1743 · Cited by 503 · see citing works
DETERMINATION OF DISCOUNT FUNCTIONS IN RATS WITH AN ADJUSTING‐AMOUNT PROCEDURE
Richards, J. B., Mitchell, S. H., de Wit, H., & Seiden, L. S. (1997) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1997.67-353 · Cited by 493 · see citing works
Dopamine: generalization and bonuses
Kakade, S. M., & Dayan, P. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00048-5 · Cited by 477 · see citing works
Richfield, E. K., Penney, J. B., & Young, A. B. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90168-1 · Cited by 448 · see citing works
Influence of Reward Delays on Responses of Dopamine Neurons
Kobayashi, S., & Schultz, W. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1600-08.2008 · Cited by 431 · see citing works
Self-citationPan, W.-X., Schmidt, R., Wickens, J. R., & Hyland, B. I. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1478-05.2005 · Cited by 429 · see citing works
Zweifel, L. S., Parker, J. G., Lobb, C. J., Rainwater, A., Wall, V. Z., Fadok, J. P., Darvas, M., Kim, M. J., Mizumori, S. J. Y., Paladini, C. A., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813415106 · Cited by 426 · see citing works
Romo, R., & Schultz, W. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.3.592 · Cited by 353 · cited 1× · see citing works
“Dopamine neurons show activations ('excitations') following reward predicting visual, auditory and somatosensory stimuli (Figure 1B) [31-33].”
BackgroundSelf-citationReal-time chemical responses in the nucleus accumbens differentiate rewarding and aversive stimuli
Roitman, M. F., Wheeler, R. A., Wightman, R. M., & Carelli, R. M. (2008) · Nature Neuroscience · doi:10.1038/nn.2219 · Cited by 343 · see citing works
Schultz, W., & Romo, R. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.3.607 · Cited by 334 · cited 5× · see citing works
“By contrast, the immediately following response component detects the true nature of the event through its graded activation with reward value [43] and its frequent depression with unrewarded and aversive stimuli [27,29,32,33] (Figure 1E).”
BackgroundInfluentialSelf-citationThe temporal precision of reward prediction in dopamine neurons
Fiorillo, C. D., Newsome, W. T., & Schultz, W. (2008) · Nature Neuroscience · doi:10.1038/nn.2159 · Cited by 310 · see citing works
Self-citationCoding of Predicted Reward Omission by Dopamine Neurons in a Conditioned Inhibition Paradigm
Tobler, P. N., Dickinson, A., & Schultz, W. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-32-10402.2003 · Cited by 300 · see citing works
Self-citationCorrelated Coding of Motivation and Outcome of Decision by Dopamine Neurons
Satoh, T., Nakai, S., Sato, T., & Kimura, M. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-30-09913.2003 · Cited by 298 · see citing works
Suri, R. E., & Schultz, W. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00697-6 · Cited by 294 · see citing works
Self-citationSelective association and conditioning
Kamin, L. J. (1969) · Medical Entomology and Zoology · Cited by 285 · see citing works
Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat
Horvitz, J. C., Stewart, T., & Jacobs, B. L. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00265-5 · Cited by 283 · see citing works
Dopamine Neurons Can Represent Context-Dependent Prediction Error
Nakahara, H., Itoh, H., Kawagoe, R., Takikawa, Y., & Hikosaka, O. (2004) · Neuron · doi:10.1016/s0896-6273(03)00869-9 · Cited by 276 · see citing works
Joshua, M., Adler, A., Mitelman, R., Vaadia, E., & Bergman, H. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3839-08.2008 · Cited by 273 · see citing works
Human substantia nigra neurons encode unexpected financial rewards
Zaghloul, K. A., Blanco, J. A., Weidemann, C. T., McGill, K., Jaggi, J. L., Baltuch, G. H., & Kahana, M. J. (2009) · Science · doi:10.1126/science.1167342 · Cited by 264 · see citing works
Synaptic plasticity and drug addiction
Jones, S., & Bonci, A. (2004) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2004.08.011 · Cited by 245 · see citing works
Guarraci, F. A., & Kapp, B. S. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00102-8 · Cited by 201 · see citing works
Statistics of Midbrain Dopamine Neuron Spike Trains in the Awake Primate
Bayer, H. M., Lau, B., & Glimcher, P. W. (2007) · Journal of Neurophysiology · doi:10.1152/jn.01140.2006 · Cited by 184 · see citing works
Schultz, W., & Romo, R. (1987) · Journal of Neurophysiology · doi:10.1152/jn.1987.57.1.201 · Cited by 184 · cited 1× · see citing works
“Aversive stimulation in anaesthetised animals produces varying but often low degrees of mostly slower, activating responses (50% [47]; 18% [48]; 17% [49]; 14% [50]) and often depressions of activity.”
BackgroundSelf-citationChiodo, L. A., Antelman, S. M., Caggiula, A. R., & Lineberry, C. G. (1980) · Brain Research · doi:10.1016/0006-8993(80)90366-2 · Cited by 179 · see citing works
Mantz, J., Thierry, A. M., & Glowinski, J. (1989) · Brain Research · doi:10.1016/0006-8993(89)91263-8 · Cited by 168 · see citing works
Wise, R. A. (1989) · Annual Review of Psychology · doi:10.1146/annurev.psych.40.1.191 · Cited by 164 · see citing works
Adjusting delay to reinforcement: Comparing choice in pigeons and humans.
Rodríguez, M., & Logue, A. W. (1988) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.14.1.105 · Cited by 158 · see citing works
Adding prediction risk to the theory of reward learning
PREUSCHOFF, K., & BOSSAERTS, P. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1390.005 · Cited by 133 · cited 1× · see citing works
“Theoretical considerations suggest that error teaching signals that are scaled by variance or standard deviation rather than mean can mediate stable learning that is resistant to the predicted risk of outcomes [30].”
Adjusting delay to reinforcement: Comparing choice in pigeons and humans.
Rodriguez, M. L., & Logue, A. W. (1988) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.14.1.105 · Cited by 129 · see citing works
Responses of monkey midbrain dopamine neurons during delayed alternation performance
Ljungberg, T., Apicella, P., & Schultz, W. (1991) · Brain Research · doi:10.1016/0006-8993(91)90816-e · Cited by 128 · see citing works
Self-citationYoung, A. M. J. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2004.03.003 · Cited by 123 · see citing works
Strecker, R., & Jacobs, B. (1985) · Brain Research · doi:10.1016/0006-8993(85)91304-6 · Cited by 115 · see citing works
Brown, M. T. C., Henny, P., Bolam, J. P., & Magill, P. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4423-08.2009 · Cited by 106 · see citing works
Harnett, M. T., Bernier, B. E., Ahn, K.-C., & Morikawa, H. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.011 · Cited by 103 · see citing works
Coizet, V., Dommett, E. J., Redgrave, P., & Overton, P. G. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.01.030 · Cited by 92 · see citing works
Takikawa, Y., Kawagoe, R., & Hikosaka, O. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00238.2004 · Cited by 82 · see citing works
Sheafor, P. J. (1975) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.1.3.245 · Cited by 65 · see citing works
Blythe, S. G., Atherton, J. F., & Bevan, M. D. (2007) · Journal of Neurophysiology · doi:10.1152/jn.01157.2006 · Cited by 62 · see citing works
Sheafor, P. J. (1975) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.1.3.245 · Cited by 37 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dopamine in motivational control: rewarding, aversive, and alerting
Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.022 · Cited by 2,396 · see citing works
The mysterious motivational functions of mesolimbic dopamine
Salamone, J. D., & Correa, M. (2012) · Neuron · doi:10.1016/j.neuron.2012.10.021 · Cited by 1,418 · see citing works
Reward, dopamine and the control of food intake: implications for obesity
Volkow, N. D., Wang, G.-J., & Baler, R. D. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.11.001 · Cited by 1,400 · see citing works
Wulf, G., & Lewthwaite, R. (2016) · Psychonomic Bulletin & Review · doi:10.3758/s13423-015-0999-9 · Cited by 1,238 · see citing works
Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons
Chaudhury, D., Walsh, J. J., Friedman, A. K., Juarez, B., Ku, S. M., Koo, J. W., Ferguson, D., Tsai, H.-C., Pomeranz, L., Christoffel, D. J., et al. (2013) · Nature · doi:10.1038/nature11713 · Cited by 1,156 · see citing works
Peers increase adolescent risk taking by enhancing activity in the brain’s reward circuitry
Chein, J., Albert, D., O’Brien, L., Uckert, K., & Steinberg, L. (2011) · Developmental Science · doi:10.1111/j.1467-7687.2010.01035.x · Cited by 1,180 · see citing works
“Regions in this brain pathway (especially the NAcc), which is implicated in the valuation and prediction of potential rewards (Breiter & Rosen, 1999; Delgado, 2007; O’Doherty, 2004; Schultz, 2010), have been found in several recent functional neuroimaging studies to show especially heightened activation during adolesc…”
Addiction: Beyond dopamine reward circuitry
Volkow, N. D., Wang, G.-J., Fowler, J. S., Tomasi, D., & Telang, F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010654108 · Cited by 959 · see citing works
Striatal Dopamine Release Is Triggered by Synchronized Activity in Cholinergic Interneurons
Threlfell, S., Lalic, T., Platt, N. J., Jennings, K. A., Deisseroth, K., & Cragg, S. J. (2012) · Neuron · doi:10.1016/j.neuron.2012.04.038 · Cited by 845 · see citing works
Obesity and addiction: Neurobiological overlaps
Volkow, N. D., Wang, G. ‐., Tomasi, D., & Baler, R. D. (2013) · Obesity Reviews · doi:10.1111/j.1467-789x.2012.01031.x · Cited by 800 · see citing works
Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli
Lammel, S., Ion, D. I., Roeper, J., & Malenka, R. C. (2011) · Neuron · doi:10.1016/j.neuron.2011.03.025 · Cited by 766 · see citing works
Serotonin and brain function: a tale of two receptors
Carhart-Harris, R., & Nutt, D. (2017) · Journal of Psychopharmacology · doi:10.1177/0269881117725915 · Cited by 739 · see citing works
Updating dopamine reward signals
Schultz, W. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.11.012 · Cited by 651 · see citing works
Self-citationAddiction circuitry in the human brain
Volkow, N. D., Wang, G.-J., Fowler, J. S., & Tomasi, D. (2012) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010611-134625 · Cited by 592 · see citing works
Ashok, A. H., Marques, T. R., Jauhar, S., Nour, M. M., Goodwin, G. M., Young, A. H., & Howes, O. D. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.16 · Cited by 546 · see citing works
Food and Drug Reward: Overlapping Circuits in Human Obesity and Addiction
Volkow, N. D., Wang, G. J., Fowler, J. S., Tomasi, D., & Baler, R. (2011) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2011_169 · Cited by 525 · see citing works
A neural reward prediction error revealed by a meta-analysis of ERPs using great grand averages
Sambrook, T. D., & Goslin, J. (2015) · Psychological Bulletin · doi:10.1037/bul0000006 · Cited by 411 · see citing works
Bello, E. P., Mateo, Y., Gelman, D. M., Noaín, D., Shin, J. H., Low, M. J., Alvarez, V. A., Lovinger, D. M., & Rubinstein, M. (2011) · Nature Neuroscience · doi:10.1038/nn.2862 · Cited by 364 · see citing works
Reward, addiction, withdrawal to nicotine
De Biasi, M., & Dani, J. A. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113734 · Cited by 366 · see citing works
“Liking” and “wanting” in eating and food reward: Brain mechanisms and clinical implications
Morales, I., & Berridge, K. C. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113152 · Cited by 346 · see citing works
Navratilova, E., Xie, J. Y., Okun, A., Qu, C., Eyde, N., Ci, S., Ossipov, M. H., King, T., Fields, H. L., & Porreca, F. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214605109 · Cited by 313 · see citing works
What, If, and When to Move: Basal Ganglia Circuits and Self-Paced Action Initiation
Klaus, A., Alves da Silva, J., & Costa, R. M. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031033 · Cited by 284 · see citing works
Action versus valence in decision making
Guitart-Masip, M., Duzel, E., Dolan, R., & Dayan, P. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2014.01.003 · Cited by 270 · see citing works
Hu, H. (2016) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-014106 · Cited by 253 · see citing works
Dopaminergic basis of salience dysregulation in psychosis
Winton-Brown, T. T., Fusar-Poli, P., Ungless, M. A., & Howes, O. D. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2013.11.003 · Cited by 231 · see citing works
Reinforcement learning in depression: a review of computational research
Chen, C., Takahashi, T., Nakagawa, S., Inoue, T., & Kusumi, I. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.05.005 · Cited by 233 · see citing works
Aberrant learning and memory in addiction
Torregrossa, M. M., Corlett, P. R., & Taylor, J. R. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.02.014 · Cited by 223 · see citing works
Mesolimbic Dopamine and the Regulation of Motivated Behavior
Salamone, J. D., Pardo, M., Yohn, S. E., López-Cruz, L., SanMiguel, N., & Correa, M. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2015_383 · Cited by 204 · see citing works
Mechanisms for widespread hippocampal involvement in cognition.
Shohamy, D., & Turk-Browne, N. B. (2013) · Journal of Experimental Psychology: General · doi:10.1037/a0034461 · Cited by 187 · see citing works
Prediction error associated with the perceptual segmentation of naturalistic events
Zacks, J. M., Kurby, C. A., Eisenberg, M. L., & Haroutunian, N. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00078 · Cited by 202 · see citing works
Is internet pornography causing sexual dysfunctions? A review with clinical reports
Park, B., Wilson, G., Berger, J., Christman, M., Reina, B., Bishop, F., Klam, W., & Doan, A. (2016) · Behavioral Sciences · doi:10.3390/bs6030017 · Cited by 187 · see citing works
Altered neural reward and loss processing and prediction error signalling in depression
Ubl, B., Kuehner, C., Kirsch, P., Ruttorf, M., Diener, C., & Flor, H. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsu158 · Cited by 165 · see citing works
Social deprivation enhances VTA synaptic plasticity and drug-induced contextual learning
Whitaker, L. R., Degoulet, M., & Morikawa, H. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.022 · Cited by 177 · see citing works
Anterior cingulate is a source of valence-specific information about value and uncertainty
Monosov, I. E. (2017) · Nature Communications · doi:10.1038/s41467-017-00072-y · Cited by 163 · see citing works
Peake, S. J., Dishion, T. J., Stormshak, E. A., Moore, W. E., & Pfeifer, J. H. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.05.061 · Cited by 147 · see citing works
Sensation-seeking: dopaminergic modulation and risk for psychopathology
Norbury, A., & Husain, M. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.04.015 · Cited by 142 · see citing works
Weeland, J., Overbeek, G., de Castro, B. O., & Matthys, W. (2015) · Clinical Child and Family Psychology Review · doi:10.1007/s10567-015-0196-4 · Cited by 138 · see citing works
Kim, U., & Lee, T. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08030.x · Cited by 133 · see citing works
Putting desire on a budget: dopamine and energy expenditure, reconciling reward and resources
Beeler, J. A., Frazier, C. R. M., & Zhuang, X. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2012.00049 · Cited by 136 · see citing works
Doremus-Fitzwater, T. L., & Spear, L. P. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.015 · Cited by 125 · see citing works
Ziegler, S., Pedersen, M. L., Mowinckel, A. M., & Biele, G. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.09.002 · Cited by 110 · see citing works
Bast, N., Poustka, L., & Freitag, C. M. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13795 · Cited by 121 · see citing works
Neuroendocrinology of Parental Response to Baby‐Cry
Swain, J. E., Kim, P., & Ho, S. S. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02212.x · Cited by 106 · see citing works
Aversive stimuli and loss in the mesocorticolimbic dopamine system
Brooks, A. M., & Berns, G. S. (2013) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.04.001 · Cited by 85 · see citing works
Sleep and dreaming are for important matters
Perogamvros, L., Dang-Vu, T. T., Desseilles, M., & Schwartz, S. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00474 · Cited by 77 · see citing works
Bernacer, J., Corlett, P. R., Ramachandra, P., McFarlane, B., Turner, D. C., Clark, L., Robbins, T. W., Fletcher, P. C., & Murray, G. K. (2013) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2013.12070978 · Cited by 77 · see citing works
Anterior insula reflects surprise in value-based decision-making and perception
Loued-Khenissi, L., Pfeuffer, A., Einhäuser, W., & Preuschoff, K. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116549 · Cited by 66 · see citing works
Shomrat, T., Turchetti-Maia, A. L., Stern-Mentch, N., Basil, J. A., & Hochner, B. (2015) · Journal of Comparative Physiology A · doi:10.1007/s00359-015-1023-6 · Cited by 73 · see citing works
Balancing new against old information: the role of puzzlement surprise in learning
Faraji, M., Preuschoff, K., & Gerstner, W. (2018) · Neural Computation · doi:10.1162/neco_a_01025 · Cited by 68 · see citing works
Mechanistic insights into nicotine withdrawal
Paolini, M., & De Biasi, M. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2011.07.075 · Cited by 66 · see citing works
“The DA released encodes reward prediction errors and incentive salience and provides a learning signal for the optimization of goal-directed behavior [31,32].”
Wotruba, D., Heekeren, K., Michels, L., Buechler, R., Simon, J. J., Theodoridou, A., Kollias, S., Rössler, W., & Kaiser, S. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00382 · Cited by 61 · see citing works
Lahey, B. B., Rathouz, P. J., Lee, S. S., Chronis-Tuscano, A., Pelham, W. E., Waldman, I. D., & Cook, E. H. (2011) · Journal of Abnormal Psychology · doi:10.1037/a0021133 · Cited by 63 · see citing works
Nock, N. L., Minnes, S., & Alberts, J. L. (2017) · Birth Defects Research · doi:10.1002/bdr2.1182 · Cited by 61 · see citing works
Robinson, J. E., Coughlin, G. M., Hori, A. M., Cho, J. R., Mackey, E. D., Turan, Z., Patriarchi, T., Tian, L., & Gradinaru, V. (2019) · eLife · doi:10.7554/elife.48983 · Cited by 44 · see citing works
Segovia, K. N., Correa, M., & Salamone, J. D. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.07.078 · Cited by 44 · see citing works
Neural circuitry of novelty salience processing in psychosis risk: Association with clinical outcome
Modinos, G., Allen, P., Zugman, A., Dima, D., Azis, M., Samson, C., Bonoldi, I., Quinn, B., Gifford, G. W. G., Smart, S. E., et al. (2020) · Schizophrenia Bulletin · doi:10.1093/schbul/sbz089 · Cited by 31 · see citing works
Pharmacotherapy for Neuropsychiatric Symptoms in Frontotemporal Dementia
Le, C., & Finger, E. (2021) · CNS Drugs · doi:10.1007/s40263-021-00854-5 · Cited by 26 · see citing works
Mesolimbic Dopamine and Habenulo-Interpeduncular Pathways in Nicotine Withdrawal
Dani, J. A., & De Biasi, M. (2013) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a012138 · Cited by 34 · see citing works
Stressful Events as Teaching Signals for the Brain
Trapp, S., O’Doherty, J. P., & Schwabe, L. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.03.007 · Cited by 25 · see citing works
Ventral striatum dopamine release encodes unique properties of visual stimuli in mice
Gonzalez, L. S., Fisher, A. A., D'Souza, S. P., Cotella, E. M., Lang, R. A., & Robinson, J. E. (2023) · eLife · doi:10.7554/elife.85064 · Cited by 18 · see citing works
- Authors
- Schultz, W.
- Affiliations
- University of Cambridge (GB)
- Corresponding author
- Schultz, Wolfram
- ORCID
- Schultz, Wolfram
- Venue
- Behavioral and Brain Functions
- Published
- 2010
- Volume
- 6
- Issue
- 1
- Pages
- 24
- ISSN
- 1744-9081 (ISSN-L)
- PMC
- PMC2876988
- OpenAlex
- W2156581621
- Cited by
- 653
- References
- 70
- Citations by year
- 2026: 16 · 2025: 19 · 2024: 26 · 2023: 25 · 2022: 22 · 2021: 24 · 2020: 35 · 2019: 31 · 2018: 45 · 2017: 44 · 2016: 44 · 2015: 63 · 2014: 46 · 2013: 65 · 2012: 74
- FWCI
- 6.11
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Behavioral and Brain Functions (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Funders
- National Science Foundation
- Wellcome Trust (095495)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- dopaminergic neurons, reward value, risk, prediction error, midbrain dopamine system, punishment, novelty, economic decision-making, expected value, single-unit recording
- MeSH terms
- Animals, Haplorhini, Behavior, Animal, Conditioning, Psychological, Dopamine, Neurons, Reward, Risk-Taking
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review