Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli
Abstract
Midbrain dopamine systems are crucially involved in motivational processes underlying the learning and execution of goal-directed behaviour. Dopamine neurons in monkeys are uniformly activated by unpredicted appetitive stimuli such as food and liquid rewards and conditioned, reward-predicting stimuli. By contrast, fully predicted stimuli are ineffective, and the omission of predicted reward depresses their activity. These characteristics follow associative-learning rules, suggesting that dopamine responses report an error in reward prediction. Accordingly, neural network models are efficiently trained using a dopamine-like reinforcement signal. However, it is unknown whether the responses to environmental stimuli concern specific motivational attributes or reflect more general stimulus salience. To resolve this, we have compared dopamine impulse responses to motivationally opposing appetitive and aversive stimuli. In contrast to appetitive events, primary and conditioned non-noxious aversive stimuli either failed to activate dopamine neurons or, in cases of close resemblance with appetitive stimuli, induced weaker responses than appetitive stimuli. Thus, dopamine neurons preferentially report environmental stimuli with appetitive rather than aversive motivational value.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
In responding to infant social cues, mothers need to integrate affective and cognitive information about their baby, and evaluate competing demands, before choosing the most appropriate behavioral response.
“In responding to infant social cues, whether positive or negative, mothers need to integrate both affective and cognitive information about their baby, and evaluate competing demands, before choosing the most appropriate behavioral response (52;53).”
From What’s in a smile? Maternal brain responses to infant facial cues (2008) · cites this paper as [53]
Previously reported activations of dopamine neurons by punishers may have been due to physical impact of the tested stimuli, rather than true aversiveness.
“Thus, it is possible that the previously reported activations of dopamine neurons by punishers15,17,19,21–24,134 may have been due to physical impact of the tested stimuli, rather than true aversiveness.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [19]
Phasic dopamine activations by aversive stimuli constitute the initial, unselective dopamine response component driven by physical impact, possibly boosted by reward context and reward generalization, rather than reflecting a straightforward aversive response.
“The phasic dopamine activations by aversive stimuli seem to constitute the initial, unselective dopamine response component driven by physical impact25, and possibly boosted by reward context and reward generalization19, rather than reflecting a straightforward aversive response”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [19]
Some studies have reported that aversive stimuli inhibit DA activity of midbrain neurons, whereas others have found that they elicit phasic DA release in the VS.
“whereas some studies have reported that aversive stimuli inhibit the DA activity of midbrain neurons (e.g., [67]), others have found that they elicit phasic DA release in the VS (e.g., [68]).”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [67]
Cites
The neural basis of drug craving: An incentive-sensitization theory of addiction
Robinson, T. (1993) · Brain Research Reviews · doi:10.1016/0165-0173(93)90013-p · Cited by 7,346 · see citing works
Classical conditioning II: Current research and theory.
Black, A. H., & Prokasy, W. F. (1972) · Appleton-Century-Crofts eBooks · Cited by 4,449 · 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
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-citationModels of Information Processing in the Basal Ganglia
(1994) · doi:10.7551/mitpress/4708.001.0001 · Cited by 1,190 · see citing works
Abercrombie, E. D., Keefe, K. A., DiFrischia, D. S., & Zigmond, M. J. (1989) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1989.tb09224.x · Cited by 1,106 · see citing works
Responses 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-citationContemporary Animal Learning Theory.
Abrahamson, D. (1981) · Europe PMC (PubMed Central) · Cited by 945 · see citing works
Contemporary Animal Learning Theory
LoLordo, V. M., & Dickinson, A. (1982) · The American Journal of Psychology · doi:10.2307/1422669 · Cited by 891 · see citing works
Freund, T. F., Powell, J. F., & Smith, A. D. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90294-x · Cited by 867 · see citing works
Involvement of the amygdala in stimulus-reward associations: interaction with the ventral striatum
Cador, M., Robbins, T. W., & Everitt, B. J. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90354-0 · Cited by 652 · see citing works
Importance of unpredictability for reward responses in primate dopamine neurons
Mirenowicz, J., & Schultz, W. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.72.2.1024 · Cited by 544 · see citing works
Self-citationYung, K. K. L., Bolam, J. P., Smith, A. D., Hersch, S. M., Ciliax, B. J., & Levey, A. I. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00536-e · Cited by 543 · see citing works
Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex.
Goldman-Rakic, P. S., Leranth, C., Williams, S. M., Mons, N. E., & Geffard, M. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.22.9015 · Cited by 433 · see citing works
Romo, R., & Schultz, W. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.3.592 · Cited by 353 · see citing works
Self-citationFunctions of dopamine in the dorsal and ventral striatum
Robbins, T. W., & Everitt, B. J. (1992) · Seminars in Neuroscience · doi:10.1016/1044-5765(92)90010-y · Cited by 348 · see citing works
Nishijo, H., Ono, T., & Nishino, H. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-10-03570.1988 · Cited by 333 · see citing works
Value-dependent selection in the brain: Simulation in a synthetic neural model
Friston, K. J., Tononi, G., Reeke, G. N., Sporns, O., & Edelman, G. M. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90592-4 · Cited by 268 · see citing works
Beninger, R. J., & Hahn, B. (1983) · Science · doi:10.1126/science.6857251 · Cited by 254 · see citing works
Models of information processing in the basal Ganglia
Hikosaka, O. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)90004-7 · Cited by 248 · see citing works
Relations between movement and single cell discharge in the substantia nigra of the behaving monkey
DeLong, M., Crutcher, M., & Georgopoulos, A. (1983) · The Journal of Neuroscience · doi:10.1523/jneurosci.03-08-01599.1983 · Cited by 247 · see citing works
Chergui, K., Suaud‐Chagny, M., & Gonon, F. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90465-0 · Cited by 229 · see citing works
Amygdalectomy and disconnection in visual learning for auditory secondary reinforcement by monkeys.
Gaffan, D., & Harrison, S. (1987) · PubMed · Cited by 190 · see citing works
Schultz, W., & Romo, R. (1987) · Journal of Neurophysiology · doi:10.1152/jn.1987.57.1.201 · Cited by 184 · see citing works
Self-citationActivity of dopamine neurons in the behaving primate
Schultz, W. (1992) · Seminars in Neuroscience · doi:10.1016/1044-5765(92)90011-p · Cited by 178 · see citing works
Self-citationLouilot, A., Moal, M. L., & Simon, H. (1986) · Brain Research · doi:10.1016/0006-8993(86)90646-3 · Cited by 168 · see citing works
Detecting behaviorally relevant changes in extracellular dopamine with microdialysis
Church, W. H., Justice, J. B., & Neill, D. B. (1987) · Brain Research · doi:10.1016/0006-8993(87)91150-4 · Cited by 148 · see citing works
The activity of pars compacta neurons of the monkey substantia nigra in relation to motor activation
Schultz, W., Ruffieux, A., & Aebischer, P. (1983) · Experimental Brain Research · doi:10.1007/bf00237874 · Cited by 136 · see citing works
Self-citationYoung, A. M. J., Joseph, M. H., & Gray, J. A. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90275-7 · Cited by 111 · see citing works
Heterogeneity of evoked dopamine overflow wihin the striatal and striatoamygdaloid regions
Garris, P. A., Ciolkowski, E. L., & Wightman, R. M. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90606-8 · Cited by 75 · see citing works
Age-dependent requirements of sympathetic neurons in serum-free culture
Selak, I., Skaper, S. D., & Varon, S. S. (1983) · Developmental Brain Research · doi:10.1016/0165-3806(83)90173-6 · Cited by 29 · see citing works
Flagged first, then by citations
1 of the 33 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
An Integrative Theory of Prefrontal Cortex Function
Miller, E. K., & Cohen, J. D. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.167 · Cited by 12,803 · see citing works
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-citationPredictive 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-citationWhat is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?
Berridge, K. C., & Robinson, T. E. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00019-8 · Cited by 4,127 · see citing works
Holroyd, C. B., & Coles, M. G. H. (2002) · Psychological Review · doi:10.1037/0033-295x.109.4.679 · Cited by 4,027 · see citing works
Getting formal with dopamine and reward
Schultz, W. (2002) · Neuron · doi:10.1016/s0896-6273(02)00967-4 · Cited by 2,574 · see citing works
Self-citationDopamine 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 debate over dopamine’s role in reward: the case for incentive salience
Berridge, K. C. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0578-x · Cited by 2,347 · see citing works
Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens
Knutson, B., Adams, C. M., Fong, G. W., & Hommer, D. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-16-j0002.2001 · Cited by 2,244 · see citing works
The prefontral cortex and cognitive control
Miller, E. K. (2000) · Nature Reviews Neuroscience · doi:10.1038/35036228 · Cited by 2,016 · see citing works
Behavioral Theories and the Neurophysiology of Reward
Schultz, W. (2006) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070229 · Cited by 1,637 · see citing works
Self-citationJentsch, J. D., & Taylor, J. R. (1999) · Psychopharmacology · doi:10.1007/pl00005483 · Cited by 1,545 · see citing works
Temporal difference models and reward-related learning in the human brain
O'Doherty, J. P., Dayan, P., Friston, K., Critchley, H., & Dolan, R. J. (2003) · Neuron · doi:10.1016/s0896-6273(03)00169-7 · Cited by 1,522 · see citing works
Assessment of positive emotions in animals to improve their welfare
Boissy, A., Manteuffel, G., Jensen, M. B., Moe, R. O., Spruijt, B., Keeling, L. J., Winckler, C., Forkman, B., Dimitrov, I., Langbein, J., et al. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.02.003 · Cited by 1,486 · see citing works
A new look at habits and the habit-goal interface.
Wood, W., & Neal, D. T. (2007) · Psychological Review · doi:10.1037/0033-295x.114.4.843 · Cited by 1,470 · see citing works
Ikemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450 · see citing works
Neuronal Coding of Prediction Errors
Schultz, W., & Dickinson, A. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.473 · Cited by 1,427 · see citing works
Self-citationMultiple 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-citationFMRI visualization of brain activity during a monetary incentive delay task
Knutson, B., Westdorp, A., Kaiser, E., & Hommer, D. (2000) · NeuroImage · doi:10.1006/nimg.2000.0593 · Cited by 1,414 · see citing works
Functional imaging of neural responses to expectancy and experience of monetary gains and losses
Breiter, H. C., Aharon, I., Kahneman, D., Dale, A., & Shizgal, P. (2001) · Neuron · doi:10.1016/s0896-6273(01)00303-8 · Cited by 1,404 · see citing works
Natural neural projection dynamics underlying social behavior
Gunaydin, L. A., Grosenick, L., Finkelstein, J. C., Kauvar, I. V., Fenno, L. E., Adhikari, A., Lammel, S., Mirzabekov, J. J., Airan, R. D., Zalocusky, K. A., et al. (2014) · Cell · doi:10.1016/j.cell.2014.05.017 · Cited by 1,389 · 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
Dissociation of reward anticipation and outcome with event-related fMRI
Knutson, B., Fong, G. W., Adams, C. M., Varner, J. L., & Hommer, D. (2001) · Neuroreport · doi:10.1097/00001756-200112040-00016 · Cited by 1,300 · see citing works
Multiple reward signals in the brain
Schultz, W. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044563 · Cited by 1,303 · see citing works
Self-citationAcute effects of cocaine on human brain activity and emotion
Breiter, H. C., Gollub, R. L., Weisskoff, R. M., Kennedy, D. N., Makris, N., Berke, J. D., Goodman, J. M., Kantor, H. L., Gastfriend, D. R., Riorden, J. P., et al. (1997) · Neuron · doi:10.1016/s0896-6273(00)80374-8 · Cited by 1,270 · see citing works
Changes in brain activity related to eating chocolate: From pleasure to aversion
Small, D. M. (2001) · Brain · doi:10.1093/brain/124.9.1720 · Cited by 1,179 · see citing works
Neuronal Reward and Decision Signals: From Theories to Data
Schultz, W. (2015) · Physiological Reviews · doi:10.1152/physrev.00023.2014 · Cited by 1,126 · see citing works
Self-citationDopamine 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-citationNeural responses during anticipation of a primary taste reward
O'Doherty, J. P., Deichmann, R., Critchley, H. D., & Dolan, R. J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00603-7 · Cited by 1,076 · see citing works
Circuit architecture of VTA dopamine neurons revealed by systematic input-output mapping
Beier, K. T., Steinberg, E. E., DeLoach, K. E., Xie, S., Miyamichi, K., Schwarz, L., Gao, X. J., Kremer, E. J., Malenka, R. C., & Luo, L. (2015) · Cell · doi:10.1016/j.cell.2015.07.015 · Cited by 1,068 · see citing works
Dopamine reward prediction-error signalling: A two-component response
Schultz, W. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.26 · Cited by 1,036 · see citing works
Self-citationSchultz, W. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.03.007 · Cited by 1,028 · see citing works
Self-citationNucleus accumbens shell and core dopamine: differential role in behavior and addiction
Di Chiara, G. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00286-3 · Cited by 996 · see citing works
The dopamine hypothesis of reward: past and current status
Spanagel, R., & Weiss, F. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01447-2 · Cited by 967 · see citing works
Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events
Horvitz, J. C. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00019-1 · Cited by 967 · see citing works
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
Reward processing in primate orbitofrontal cortex and basal ganglia
Schultz, W. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.272 · Cited by 942 · see citing works
Self-citationAdolescence as a neurobiological critical period for the development of higher-order cognition
Larsen, B., & Luna, B. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.005 · Cited by 853 · see citing works
A cellular mechanism of reward-related learning
Reynolds, J. N. J., Hyland, B. I., & Wickens, J. R. (2001) · Nature · doi:10.1038/35092560 · Cited by 879 · see citing works
Schwaerzel, M., Monastirioti, M., Scholz, H., Friggi-Grelin, F., Birman, S., & Heisenberg, M. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-33-10495.2003 · Cited by 871 · see citing works
Reward and aversion in a heterogeneous midbrain dopamine system
Lammel, S., Lim, B. K., & Malenka, R. C. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.03.019 · Cited by 804 · see citing works
Opponent interactions between serotonin and dopamine
Daw, N. D., Kakade, S., & Dayan, P. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00052-7 · Cited by 844 · see citing works
Phasic 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
Intact-brain analyses reveal distinct information carried by SNc dopamine subcircuits
Lerner, T. N., Shilyansky, C., Davidson, T. J., Evans, K. E., Beier, K. T., Zalocusky, K. A., Crow, A. K., Malenka, R. C., Luo, L., Tomer, R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.07.014 · Cited by 794 · see citing works
“Seminal early studies into the information encoded by midbrain DA neurons suggested that a key function of DA is to transmit reward prediction error signals (Mirenowicz and Schultz, 1996; Schultz et al., 1997; Waelti et al., 2001), a hypothesis concordant with temporal difference learning models (Montague et al.”
ResultUniform Inhibition of Dopamine Neurons in the Ventral Tegmental Area by Aversive Stimuli
Ungless, M. A., Magill, P. J., & Bolam, J. P. (2004) · Science · doi:10.1126/science.1093360 · Cited by 782 · see citing works
Dopamine neurons and their role in reward mechanisms
Schultz, W. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80007-4 · Cited by 769 · see citing works
Self-citationProjection-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
Dissociable Neural Responses in Human Reward Systems
Elliott, R., Friston, K. J., & Dolan, R. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06159.2000 · Cited by 740 · see citing works
Reinforcement learning in the brain
Niv, Y. (2009) · Journal of Mathematical Psychology · doi:10.1016/j.jmp.2008.12.005 · Cited by 724 · see citing works
Predictability modulates human brain response to reward
Berns, G. S., McClure, S. M., Pagnoni, G., & Montague, P. R. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02793.2001 · Cited by 711 · see citing works
Jhou, T. C., Fields, H. L., Baxter, M. G., Saper, C. B., & Holland, P. C. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.001 · Cited by 696 · see citing works
BOLD responses reflecting dopaminergic signals in the human ventral tegmental area
D'Ardenne, K., McClure, S. M., Nystrom, L. E., & Cohen, J. D. (2008) · Science · doi:10.1126/science.1150605 · Cited by 661 · see citing works
Dopamine signals for reward value and risk: basic and recent data
Schultz, W. (2010) · Behavioral and Brain Functions · doi:10.1186/1744-9081-6-24 · Cited by 653 · see citing works
Self-citationUpdating 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-citationDopamine reward prediction error coding
Schultz, W. (2016) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2016.18.1/wschultz · Cited by 597 · see citing works
Self-citationActivation of VTA GABA Neurons Disrupts Reward Consumption
van Zessen, R., Phillips, J. L., Budygin, E. A., & Stuber, G. D. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.016 · Cited by 620 · see citing works
Alcaro, A., Huber, R., & Panksepp, J. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.07.014 · Cited by 613 · see citing works
Gr�sser, S. M., Wrase, J., Klein, S., Hermann, D., Smolka, M. N., Ruf, M., Weber-Fahr, W., Flor, H., Mann, K., Braus, D. F., et al. (2004) · Psychopharmacology · doi:10.1007/s00213-004-1828-4 · Cited by 598 · see citing works
Temporal difference models describe higher-order learning in humans
Seymour, B., O'Doherty, J. P., Dayan, P., Koltzenburg, M., Jones, A. K., Dolan, R. J., Friston, K. J., & Frackowiak, R. S. (2004) · Nature · doi:10.1038/nature02581 · Cited by 605 · see citing works
Individual Differences in Reward Drive Predict Neural Responses to Images of Food
Beaver, J. D., Lawrence, A. D., van Ditzhuijzen, J., Davis, M. H., Woods, A., & Calder, A. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0350-06.2006 · Cited by 594 · see citing works
Hikida, T., Kimura, K., Wada, N., Funabiki, K., & Nakanishi, S. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.011 · Cited by 592 · see citing works
Schroll, C., Riemensperger, T. D., Bucher, D. B., Ehmer, J., Völler, T., Erbguth, K., Gerber, B., Hendel, T., Nagel, G., Buchner, E., et al. (2006) · Current Biology · doi:10.1016/j.cub.2006.07.023 · Cited by 587 · see citing works
An Integrative Model of the Maturation of Cognitive Control
Luna, B., Marek, S., Larsen, B., Tervo-Clemmens, B., & Chahal, R. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034054 · Cited by 550 · see citing works
How Addictive Drugs Disrupt Presynaptic Dopamine Neurotransmission
Sulzer, D. L. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.010 · Cited by 573 · see citing works
From waking to sleeping: neuronal and chemical substrates
Jones, B. E. (2005) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2005.09.009 · Cited by 577 · see citing works
Striatal circuits for reward learning and decision-making
Cox, J., & Witten, I. B. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0189-2 · Cited by 554 · see citing works
Baliki, M. N., Geha, P., Fields, H. L., & Apkarian, A. V. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.002 · Cited by 549 · see citing works
Representation of negative motivational value in the primate lateral habenula
Matsumoto, M., & Hikosaka, O. (2009) · Nature Neuroscience · doi:10.1038/nn.2233 · Cited by 547 · see citing works
Walsh, M. M., & Anderson, J. R. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.05.008 · Cited by 541 · see citing works
Dopamine-dependent plasticity of corticostriatal synapses
Reynolds, J. N. J., & Wickens, J. R. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00045-x · Cited by 528 · see citing works
Jones, B. E. (2003) · Frontiers in bioscience · doi:10.2741/1074 · Cited by 532 · see citing works
Hammer, M., & Menzel, R. (1998) · Learning & Memory · doi:10.1101/lm.5.1.146 · Cited by 530 · see citing works
Belin, D., Jonkman, S., Dickinson, A., Robbins, T. W., & Everitt, B. J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.09.027 · Cited by 520 · see citing works
Cachope, R., Mateo, Y., Mathur, B. N., Irving, J. M., Wang, H., Morales, M., Lovinger, D. M., & Cheer, J. F. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.05.011 · Cited by 519 · see citing works
A Neural Circuit Mechanism for Encoding Aversive Stimuli in the Mesolimbic Dopamine System
de Jong, J. W., Afjei, S. A., Dorocic, I. P., Peck, J. R., Liu, C. J., Kim, C. K., Tian, L., Deisseroth, K. A., & Lammel, S. (2018) · Neuron · doi:10.1016/j.neuron.2018.11.005 · Cited by 506 · see citing works
Mesolimbic dopaminergic pathways in fear conditioning
Pezze, M. A., & Feldon, J. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.09.004 · Cited by 510 · see citing works
How prediction errors shape perception, attention, and motivation
den Ouden, H. E. M., Kok, P., & de Lange, F. P. (2012) · Frontiers in Psychology · doi:10.3389/fpsyg.2012.00548 · Cited by 512 · see citing works
Is the short-latency dopamine response too short to signal reward error?
Redgrave, P., Prescott, T. J., & Gurney, K. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01373-3 · Cited by 506 · see citing works
Swain, J. E., Lorberbaum, J. P., Kose, S., & Strathearn, L. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2007.01731.x · Cited by 499 · see citing works
Tripp, G., & Wickens, J. R. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.07.026 · Cited by 492 · see citing works
Relapse to cocaine-seeking after hippocampal theta burst stimulation
Vorel, S. R., Liu, X., Hayes, R. J., Spector, J. A., & Gardner, E. L. (2001) · Science · doi:10.1126/science.1058043 · Cited by 486 · 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
A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP
Lisman, J., Grace, A. A., & Duzel, E. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.07.006 · Cited by 465 · see citing works
Burst firing in midbrain dopaminergic neurons
Overton, P. G., & Clark, D. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00039-8 · Cited by 466 · see citing works
Direct Activation of the Ventral Striatum in Anticipation of Aversive Stimuli
Jensen, J., McIntosh, A. R., Crawley, A. P., Mikulis, D. J., Remington, G., & Kapur, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00724-4 · Cited by 455 · see citing works
What’s in a smile? Maternal brain responses to infant facial cues
Strathearn, L., Li, J., Fonagy, P., & Montague, P. R. (2008) · Pediatrics · doi:10.1542/peds.2007-1566 · Cited by 460 · see citing works
Opponency revisited: competition and cooperation between dopamine and serotonin
Boureau, Y.-L., & Dayan, P. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.151 · Cited by 456 · see citing works
Roitman, M. F., Wheeler, R. A., & Carelli, R. M. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.055 · Cited by 453 · see citing works
PHARMACOLOGICAL ASPECTS OF HUMAN AND CANINE NARCOLEPSY
Nishino, S., & Mignot, E. J.-M. (1997) · Progress in Neurobiology · doi:10.1016/s0301-0082(96)00070-6 · Cited by 449 · see citing works
Neural mechanisms and temporal dynamics of performance monitoring
Ullsperger, M., Fischer, A. G., Nigbur, R., & Endraß, T. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2014.02.009 · 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
Mechanisms of cognitive set flexibility in Parkinson's disease
Cools, R. (2001) · Brain · doi:10.1093/brain/124.12.2503 · Cited by 406 · see citing works
Lisman, J. E., & Otmakhova, N. A. (2001) · Hippocampus · doi:10.1002/hipo.1071 · Cited by 402 · see citing works
Précis of <i>The brain and emotion</i>
Rolls, E. T. (2000) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00002429 · Cited by 397 · see citing works
Striatal dopamine neurotransmission: Regulation of release and uptake
Sulzer, D., Cragg, S. J., & Rice, M. E. (2016) · Basal Ganglia · doi:10.1016/j.baga.2016.02.001 · Cited by 382 · see citing works
Bassareo, V., & Chiara, G. D. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-02-00851.1997 · Cited by 375 · see citing works
Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra
French, E. D., Dillon, K. A., & Wu, X. (1997) · Neuroreport · doi:10.1097/00001756-199702100-00014 · Cited by 374 · see citing works
Dissecting the diversity of midbrain dopamine neurons
Roeper, J. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.03.003 · Cited by 372 · see citing works
Brown, M. T. C., Tan, K. R., O’Connor, E. C., Nikonenko, I., Müller, D., & Lüscher, C. (2012) · Nature · doi:10.1038/nature11657 · Cited by 368 · see citing works
A potential role for thalamocingulate circuitry in human maternal behavior
Lorberbaum, J. P., Newman, J. D., Horwitz, A. R., Dubno, J. R., Lydiard, R. B., Hamner, M. B., Bohning, D. E., & George, M. S. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01284-7 · Cited by 359 · see citing works
- Authors
- Mirenowicz, J., & Schultz, W.
- Affiliations
- University of Fribourg (CH)
- Venue
- Nature
- Published
- 1996-02
- Volume
- 379
- Issue
- 6564
- Pages
- 449-451
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1979640215
- Cited by
- 829
- References
- 33
- Citations by year
- 2026: 8 · 2025: 16 · 2024: 23 · 2023: 14 · 2022: 22 · 2021: 15 · 2020: 17 · 2019: 19 · 2018: 33 · 2017: 23 · 2016: 34 · 2015: 39 · 2014: 40 · 2013: 46 · 2012: 45
- FWCI
- 11.74
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- 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 › Memory and Neural Mechanisms
- Keywords
- midbrain dopaminergic neurons, appetitive stimuli, aversive stimuli, reward prediction error, motivational value, stimulus salience, reinforcement learning, goal-directed behavior
- MeSH terms
- Animals, Haplorhini, Appetitive Behavior, Avoidance Learning, Dopamine, Mesencephalon, Neurons
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