Multiple dopamine functions at different time courses

Schultz, Wolfram

doi:10.1146/annurev.neuro.28.061604.135722

Cited by 1,415Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesParkinson's Disease Mechanisms and Treatments

Multiple dopamine functions at different time courses

Schultz, Wolfram·2007·Annual Review of Neuroscience

DOI 10.1146/annurev.neuro.28.061604.135722

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Abstract

Many lesion studies report an amazing variety of deficits in behavioral functions that cannot possibly be encoded in great detail by the relatively small number of midbrain dopamine neurons. Although hoping to unravel a single dopamine function underlying these phenomena, electrophysiological and neurochemical studies still give a confusing, mutually exclusive, and partly contradictory account of dopamine's role in behavior. However, the speed of observed phasic dopamine changes varies several thousand fold, which offers a means to differentiate the behavioral relationships according to their time courses. Thus dopamine is involved in mediating the reactivity of the organism to the environment at different time scales, from fast impulse responses related to reward via slower changes with uncertainty, punishment, and possibly movement to the tonic enabling of postsynaptic motor, cognitive, and motivational systems deficient in Parkinson's disease.

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Neurocircuitry of Addiction
Koob, G. F., & Volkow, N. D. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.110 · Cited by 5,340 · see citing works
Inflammation and Its Discontents: The Role of Cytokines in the Pathophysiology of Major Depression
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Dopamine in motivational control: rewarding, aversive, and alerting
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A framework for studying the neurobiology of value-based decision making
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Schizophrenia
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The locus coeruleus and noradrenergic modulation of cognition
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Modulation of Striatal Projection Systems by Dopamine
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Synaptic plasticity and addiction
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Input-specific control of reward and aversion in the ventral tegmental area
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Phasic Firing in Dopaminergic Neurons Is Sufficient for Behavioral Conditioning
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Affective neuroscience of pleasure: reward in humans and animals
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Whole-Brain Mapping of Direct Inputs to Midbrain Dopamine Neurons
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Neuronal Reward and Decision Signals: From Theories to Data
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Ventral tegmental area: cellular heterogeneity, connectivity and behaviour
Morales, M., & Margolis, E. B. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.165 · Cited by 1,108 · see citing works
Dopamine reward prediction-error signalling: A two-component response
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Distinct roles for direct and indirect pathway striatal neurons in reinforcement
Kravitz, A. V., Tye, L. D., & Kreitzer, A. C. (2012) · Nature Neuroscience · doi:10.1038/nn.3100 · Cited by 972 · see citing works
Hierarchical Models in the Brain
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“In this figure, we have focused on means or expectations m i of the marginal densities, q ( W i )= N ( W i : m i , C i ). doi:10.1371/journal.pcbi.1000211.g010 have been implicated in value-learning [68–70], attention and the encoding of uncertainty [63,71].”
BackgroundInfluential
What does dopamine mean?
Berke, J. D. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0152-y · Cited by 904 · see citing works
Synaptic Plasticity Forms and Functions
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Reward and aversion in a heterogeneous midbrain dopamine system
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A common neurobiology for pain and pleasure
Leknes, S., & Tracey, I. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2333 · Cited by 784 · see citing works
The neurobiology of rewards and values in social decision making
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The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses.
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Dopamine signals for reward value and risk: basic and recent data
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Alcoholism: A Systems Approach From Molecular Physiology to Addictive Behavior
Spanagel, R. (2009) · Physiological Reviews · doi:10.1152/physrev.00013.2008 · Cited by 636 · see citing works
Motivation of extended behaviors by anterior cingulate cortex
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The Simulation of Smiles (SIMS) model: Embodied simulation and the meaning of facial expression
Niedenthal, P. M., Mermillod, M., Maringer, M., & Hess, U. (2010) · Behavioral and Brain Sciences · doi:10.1017/s0140525x10000865 · Cited by 618 · see citing works
Start/stop signals emerge in nigrostriatal circuits during sequence learning
Jin, X., & Costa, R. M. (2010) · Nature · doi:10.1038/nature09263 · Cited by 611 · see citing works
Rapid signalling in distinct dopaminergic axons during locomotion and reward
Howe, M. W., & Dombeck, D. A. (2016) · Nature · doi:10.1038/nature18942 · Cited by 597 · see citing works
VTA dopaminergic neurons regulate ethologically relevant sleep-wake behaviors
Eban-Rothschild, A., Rothschild, G., Giardino, W. J., Jones, J. R., & de Lecea, L. (2016) · Nature Neuroscience · doi:10.1038/nn.4377 · Cited by 583 · see citing works
Reward and Punishment Processing in Depression
Eshel, N., & Roiser, J. P. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.01.027 · Cited by 575 · see citing works
Dopamine neuron activity before action initiation gates and invigorates future movements
da Silva, J. A., Tecuapetla, F., Paixão, V., & Costa, R. M. (2018) · Nature · doi:10.1038/nature25457 · Cited by 550 · see citing works
Predicting Value of Pain and Analgesia: Nucleus Accumbens Response to Noxious Stimuli Changes in the Presence of Chronic Pain
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
The dopamine hypothesis of bipolar affective disorder: the state of the art and implications for treatment
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
Learning from experience: Event-related potential correlates of reward processing, neural adaptation, and behavioral choice
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 and Cognitive Control in Prefrontal Cortex
Ott, T., & Nieder, A. (2019) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.12.006 · Cited by 530 · see citing works
Physiology and pharmacology of striatal neurons
Kreitzer, A. C. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135422 · Cited by 530 · see citing works
Factors modulating neural reactivity to drug cues in addiction: a survey of human neuroimaging studies
Jasinska, A. J., Stein, E. A., Kaiser, J., Naumer, M. J., & Yalachkov, Y. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.10.013 · Cited by 513 · see citing works
Basolateral Amygdala Neurons Facilitate Reward-Seeking Behavior by Exciting Nucleus Accumbens Neurons
Ambroggi, F., Ishikawa, A., Fields, H. L., & Nicola, S. M. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.004 · Cited by 488 · see citing works
Principles of Neural Design
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Goal Representations and Motivational Drive in Schizophrenia: The Role of Prefrontal-Striatal Interactions
Barch, D. M., & Dowd, E. C. (2010) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq068 · Cited by 478 · see citing works
Memory and Brain Systems: 1969–2009
Squire, L. R. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3575-09.2009 · 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
Serotonin and dopamine: unifying affective, activational, and decision functions.
Cools, R., Nakamura, K., & Daw, N. D. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.121 · Cited by 464 · see citing works
A neurocognitive approach to understanding the neurobiology of addiction
Noël, X., Brevers, D., & Bechara, A. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.01.018 · Cited by 436 · see citing works
Dopamine: The Neuromodulator of Long-Term Synaptic Plasticity, Reward and Movement Control
Speranza, L., di Porzio, U., Viggiano, D., Donato, A. D., & Volpicelli, F. (2021) · Cells · doi:10.3390/cells10040735 · Cited by 430 · see citing works
Dopaminergic reward system: a short integrative review
Arias-Carrión, Ó., Stamelou, M., Murillo‐Rodríguez, E., Menéndez‐González, M., & Pöppel, E. (2010) · International Archives of Medicine · doi:10.1186/1755-7682-3-24 · Cited by 413 · see citing works
Robust Pacemaking in Substantia Nigra Dopaminergic Neurons
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Novelty or Surprise?
Barto, A., Mirolli, M., & Baldassarre, G. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00907 · Cited by 397 · see citing works
Separable learning systems in the macaque brain and the role of orbitofrontal cortex in contingent learning
Walton, M. E., Behrens, T. E. J., Buckley, M. J., Rudebeck, P. H., & Rushworth, M. F. S. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.027 · Cited by 397 · see citing works
The neuromodulator of exploration: A unifying theory of the role of dopamine in personality
DeYoung, C. G. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00762 · Cited by 387 · see citing works
Closed-Loop and Activity-Guided Optogenetic Control
Grosenick, L., Marshel, J. H., & Deisseroth, K. A. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.034 · Cited by 384 · see citing works
Dopaminergic Mechanisms of Reduced Basal Ganglia Responses to Hedonic Reward During Interferon Alfa Administration
Capuron, L., Pagnoni, G., Drake, D. F., Woolwine, B. J., Spivey, J. R., Crowe, R. J., Votaw, J. R., Goodman, M. M., & Miller, A. H. (2012) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.2094 · Cited by 382 · see citing works
Dopamine, affordance and active inference
Friston, K. J., Shiner, T., FitzGerald, T., Galea, J. M., Adams, R., Brown, H., Dolan, R. J., Moran, R., Stephan, K. E., & Bestmann, S. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002327 · Cited by 381 · 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
“For example, phasic burst firing is induced by unpredicted reward or unanticipated cues that have been conditioned to a known reward (Schultz 2007b, Schultz et al. 1997).”
Background
Beyond the FRN: Broadening the time-course of EEG and ERP components implicated in reward processing
Glazer, J. E., Kelley, N. J., Pornpattananangkul, N., Mittal, V. A., & Nusslock, R. (2018) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2018.02.002 · Cited by 362 · see citing works
Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior
Adamantidis, A. R., Tsai, H.-C., Boutrel, B., Zhang, F., Stuber, G. D., Budygin, E. A., Tourino, C., Bonci, A., Deisseroth, K., & de Lecea, L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2246-11.2011 · Cited by 357 · see citing works
Rewards teach visual selective attention
Chelazzi, L., Perlato, A., Santandrea, E., & Della Libera, C. (2013) · Vision Research · doi:10.1016/j.visres.2012.12.005 · Cited by 354 · see citing works
The motivation and pleasure dimension of negative symptoms: Neural substrates and behavioral outputs
Kring, A. M., & Barch, D. M. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.06.007 · Cited by 352 · see citing works
The anatomy of choice: active inference and agency
Friston, K., Schwartenbeck, P., FitzGerald, T., Moutoussis, M., Behrens, T., & Dolan, R. J. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00598 · Cited by 340 · see citing works
Phasic acetylcholine release and the volume transmission hypothesis: time to move on
Sarter, M. F., Parikh, V., & Howe, W. M. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2635 · Cited by 340 · see citing works
Proprioception and Motor Control in Parkinson's Disease
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Development of tannin-inspired antimicrobial bioadhesives
Guo, J., Sun, W., Kim, J. P., Lu, X., Li, Q., Lin, M., Mrowczynski, O., Rizk, E., Cheng, J., Qian, G., et al. (2018) · Acta Biomaterialia · doi:10.1016/j.actbio.2018.03.008 · Cited by 328 · see citing works
Gliotransmission: Beyond Black-and-White
Savtchouk, I., & Volterra, A. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.0017-17.2017 · Cited by 325 · see citing works
Dopamine neurons projecting to the posterior striatum form an anatomically distinct subclass
Menegas, W., Bergan, J. F., Ogawa, S. K., Isogai, Y., Venkataraju, K. U., Osten, P., Uchida, N., & Watabe‐Uchida, M. (2015) · eLife · doi:10.7554/elife.10032 · Cited by 324 · see citing works
Effort, anhedonia, and function in schizophrenia: Reduced effort allocation predicts amotivation and functional impairment.
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Normal Aging Induces Changes in the Brain and Neurodegeneration Progress: Review of the Structural, Biochemical, Metabolic, Cellular, and Molecular Changes
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Exposure to elevated levels of dietary fat attenuates psychostimulant reward and mesolimbic dopamine turnover in the rat
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Common brain mechanisms of chronic pain and addiction
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Spatial and temporal scales of dopamine transmission
Liu, C., Goel, P., & Kaeser, P. S. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00455-7 · Cited by 302 · see citing works
A Unified Framework for Dopamine Signals across Timescales
Kim, H. R., Malik, A. N., Mikhael, J. G., Bech, P., Tsutsui‐Kimura, I., Sun, F., Zhang, Y., Li, Y., Watabe‐Uchida, M., Gershman, S. J., et al. (2020) · Cell · doi:10.1016/j.cell.2020.11.013 · Cited by 297 · see citing works
Dopamine Is Required for Learning and Forgetting in Drosophila
Berry, J. A., Cervantes-Sandoval, I., Nicholas, E. P., & Davis, R. L. (2012) · Neuron · doi:10.1016/j.neuron.2012.04.007 · Cited by 296 · see citing works
Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data
Spear, L. P. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.08.001 · Cited by 292 · see citing works
The anatomy of choice: dopamine and decision-making.
Friston, K., Schwartenbeck, P., FitzGerald, T., Moutoussis, M., Behrens, T., & Dolan, R. J. (2014) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2013.0481 · Cited by 289 · see citing works
The hippocampal-striatal axis in learning, prediction and goal-directed behavior
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Taste, olfactory, and food reward value processing in the brain
Rolls, E. T. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.03.002 · Cited by 287 · see citing works
Establishing moderators and biosignatures of antidepressant response in clinical care (EMBARC): Rationale and design
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Reinforcement learning can account for associative and perceptual learning on a visual-decision task
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What, If, and When to Move: Basal Ganglia Circuits and Self-Paced Action Initiation
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Materials from Mussel-Inspired Chemistry for Cell and Tissue Engineering Applications
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Neuronal Mechanisms for Sleep/Wake Regulation and Modulatory Drive
Eban-Rothschild, A., Appelbaum, L., & de Lecea, L. (2018) · Neuropsychopharmacology · doi:10.1038/npp.2017.294 · Cited by 282 · see citing works
Sleep Neurobiology from a Clinical Perspective
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When pain gets stuck: the evolution of pain chronification and treatment resistance
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Prefrontal cortex mediation of cognitive enhancement in rewarding motivational contexts
Jimura, K., Locke, H., & Braver, T. S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002007107 · Cited by 278 · see citing works
Dopamine, behavioral economics, and effort
Salamone, J. D. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.013.2009 · Cited by 277 · see citing works
Dopamine, learning, and reward-seeking behavior
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Reward and the serotonergic system
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Self-citation
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Authors: Schultz, W.
Affiliations: University of Cambridge (GB)
Corresponding author: Schultz, Wolfram
ORCID: Schultz, Wolfram
Venue: Annual Review of Neuroscience
Publisher: Annual Reviews
Published: 2007-07-01
Volume: 30
Issue: 1
Pages: 259-288
ISSN: 0147-006X (ISSN-L)
1545-4126
DOI: 10.1146/annurev.neuro.28.061604.135722
OpenAlex: W2096193724
Cited by: 1,415
References: 201
Citations by year: 2026: 47 · 2025: 58 · 2024: 73 · 2023: 73 · 2022: 75 · 2021: 68 · 2020: 66 · 2019: 63 · 2018: 66 · 2017: 74 · 2016: 79 · 2015: 100 · 2014: 99 · 2013: 87 · 2012: 85
FWCI: 5.96
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust (095495)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
Keywords: dopamine, midbrain dopaminergic neurons, reward, uncertainty, punishment, motor control, cognitive function, motivation, Parkinson's disease, behavioral deficits, lesion studies
MeSH terms: Animals, Behavior, Animal, Brain, Decision Making, Dopamine, Humans, Movement, Movement Disorders, Neural Pathways, Synaptic Transmission, Reward

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