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Dopamine, Time, and Impulsivity in Humans
Open accessAbstract
Disordered dopamine neurotransmission is implicated in mediating impulsiveness across a range of behaviors and disorders including addiction, compulsive gambling, attention-deficit/hyperactivity disorder, and dopamine dysregulation syndrome. Whereas existing theories of dopamine function highlight mechanisms based on aberrant reward learning or behavioral disinhibition, they do not offer an adequate account of the pathological hypersensitivity to temporal delay that forms a crucial behavioral phenotype seen in these disorders. Here we provide evidence that a role for dopamine in controlling the relationship between the timing of future rewards and their subjective value can bridge this explanatory gap. Using an intertemporal choice task, we demonstrate that pharmacologically enhancing dopamine activity increases impulsivity by enhancing the diminutive influence of increasing delay on reward value (temporal discounting) and its corresponding neural representation in the striatum. This leads to a state of excessive discounting of temporally distant, relative to sooner, rewards. Thus our findings reveal a novel mechanism by which dopamine influences human decision-making that can account for behavioral aberrations associated with a hyperfunctioning dopamine system.
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“Interestingly, delay discounting seems to depend on the function of the ventral striatum (104) and of the PFC, including OFC (105) and its connections to the NAc (106), and is sensitive to DA manipulations (107).”
From Obesity and addiction: Neurobiological overlaps (2013) · cites this paper as [107]
In the citing paper
“Delay discounting seems to depend on the function of ventral striatum (Gregorios-Pippas et al 2009) and of the PFC, including OFC (Bjork et al 2009), and is sensitive to DA manipulations (Pine et al 2010).”
From Food and Drug Reward: Overlapping Circuits in Human Obesity and Addiction (2011) · cites this paper as Pine et al 2010
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Citations
Cites
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MethodDopaminergic modulation of impulsive decision making in the rat insular cortex
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Dopamine Modulation of Intertemporal Decision-making: Evidence from Parkinson Disease
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How Costs Influence Decision Values for Mixed Outcomes
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Arrondo, G., Aznárez‐Sanado, M., Fernández‐Seara, M. A., Goñi, J., Loayza, F. R., Salamon-Klobut, E., Heukamp, F. H., & Pastor, M. A. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.02.011 · Cited by 22
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“Based on prior relevant work [51], the following Montreal Neurological Institute (MNI) coordinates for bilateral ROIs were defined: putamen, MNI coordinates 30 −3”
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Thunderstruck: The ACDC model of flexible sequences and rhythms in recurrent neural circuits
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Striatal dopamine modulates timing of self-initiated saccades
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“Increased impulsivity might be linked with impaired time perception, such that the promotion of the subjective passage of time may facilitate early impulsive responses (Wittmann and Paulus, 2008; Pine et al., 2010).”
BackgroundThe duality of decisions and the case for impulsiveness metrics
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“Moreover,dopamine,thekeydriverof “wanting,” regulates impulsive behavior ( Pine et al. 2010 ).”
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“…(adjusting amount procedure; Helms et al., 2006) Haloperidol (2 mg, acute) ↓ DD (Wagner et al., 2020) Haloperidol (1.5 mg, acute) did not affect DD (Pine et al., 2010) Haloperidol (0.01–0.1 mg/kg, i.p., acute) ↑ DD (Boomhower & Rasmussen, 2014) Acute testosterone gel (150 mg) ↑ DD in healthy men…”
InfluentialVentral Striatal Dopamine Synthesis Capacity Predicts Financial Extravagance in Parkinson’s Disease
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“Our results are consistent with recent preclinical models of vulnerability to behavioral disinhibition and addiction proneness, and provide novel insights into the neurobiology of potential vulnerability to impulse control problems in PD and other disorders.”
BackgroundResultBrain correlates of the intrinsic subjective cost of effort in sedentary volunteers
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“Conversely, Pine and colleagues demonstrated that healthy subjects given the dopamine precursor L-dopa, which should act throughout the brain, showed consistent increases in delay discounting (Pine et al., 2010).”
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“While some studies showed similar effects following pharmacological manipulations to foster dopamine transmission [34,38] other studies have reported contrasting effects [36,119].”
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“…(dopamine antagonist), it was demonstrated that increasing dopamine led to an increase in impulsivity through temporal discounting, i.e., assigning less value to rewards further away in the future, which coincided with reduced activity in striatal and frontal regions (Pine et al., 2010).”
BackgroundGilman, T. L., Owens, W. A., George, C. M., Metzel, L., Vitela, M., Ferreira, L., Bowman, M. A., Gould, G. G., Toney, G. M., & Daws, L. C. (2019) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.119.260794 · Cited by 16
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BackgroundPersistent Inequality: A Neurosociological Perspective
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Dopamine and Gambling Disorder: Prospects for Personalized Treatment
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“While we do not dissociate these two factors in our models, past work has incorporated preferences for time and risk into the discount factor term to improve estimates of discounting in human subjects [92].”
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High monetary reward rates and caloric rewards decrease temporal persistence
Fung, B. J., Bode, S., & Murawski, C. (2017) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2016.2759 · Cited by 10
Simulating future value in intertemporal choice
Solway, A., Lohrenz, T. M., & Montague, P. R. (2017) · Scientific Reports · doi:10.1038/srep43119 · Cited by 13
Sleep-Wake State Tradeoffs, Impulsivity and Life History Theory
Miller, A. A., & Rucas, S. L. (2012) · Evolutionary Psychology · doi:10.1177/147470491201000201 · Cited by 13
The Neurobiology of Preferences
Symmonds, M., & Dolan, R. J. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-381431-9.00001-2 · Cited by 13
Self-citationUpdate on the Pharmacological Treatment of Pathological Gambling
Bullock, S. A., & Potenza, M. N. (2014) · Current Psychopharmacologye · doi:10.2174/22115560113029990008 · Cited by 12
Impulsivity and risk-seeking as Bayesian inference under dopaminergic control
Mikhael, J. G., & Gershman, S. J. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01125-z · Cited by 11
Morgan, J., Clark, D. C., Tripodis, Y., Halloran, C. S., Minsky, A., Wildman, W. J., Durso, R., & McNamara, P. (2016) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2016.07.020 · Cited by 11
Mayer, J. T., Nicolier, M., Tio, G., Mouchabac, S., Haffen, É., & Bennabi, D. (2019) · Brain Sciences · doi:10.3390/brainsci9090230 · Cited by 11
“Considering these findings, the rTMS impact on DD behavior of depressed individuals needs to be carefully assessed by further studies, since relation between increased striatal dopaminergic activity and immediacy has been previously described [12,14].”
BackgroundIodice, P., Cannito, L., Chaigneau, A., & Palumbo, R. (2022) · Scientific Reports · doi:10.1038/s41598-022-10142-x · Cited by 21
Dopamine in Parkinson’s Disease: Precise Supplementation with Motor Planning
Chen, L., & Xie, J. (2018) · Neuroscience Bulletin · doi:10.1007/s12264-018-0245-3 · Cited by 10
Aiello, M., Terenzi, D., Furlanis, G., Catalan, M., Manganotti, P., Eleopra, R., Belgrado, E., & Rumiati, R. I. (2019) · Journal of Neurology · doi:10.1007/s00415-019-09240-0 · Cited by 10
Freinhofer, D., Schwartenbeck, P., Thon, N., Eigenberger, T., Aichhorn, W., Lenger, M., Wurst, F. M., & Kronbichler, M. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00109 · Cited by 13
“We also counted the amount of SBS choices for every participant, because studies showed similar results for K and SBS choices (66).”
ResultKnauth, K., & Peters, J. (2022) · Psychophysiology · doi:10.1111/psyp.13996 · Cited by 9
Neural reward processing under dopamine agonists: Imaging
Kassubek, J., Abler, B., & Pinkhardt, E. H. (2011) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2011.06.043 · Cited by 9
A Literature Review on Holistic Well-Being and Dopamine Fasting: An Integrated Approach
Desai, D. H., Patel, J., Saiyed, F., Upadhyay, H., Kariya, P., & Patel, J. (2024) · Cureus · doi:10.7759/cureus.61643 · Cited by 9
“These theoretical possibilities are engaging as the current treatment protocol includes medicines that might become harmful in the end [4-6].”
BackgroundGibson, A. S., Keefe, K. A., & Furlong, T. M. (2020) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.173033 · Cited by 8
Temporal discounting in adolescents and adults with Tourette syndrome
Schüller, C. B., Wagner, B., Schüller, T., Baldermann, J. C., Huys, D., Koerner, J. K. A., Nießen, E., Münchau, A. M., Brandt, V. C., Peters, J., et al. (2021) · PLoS ONE · doi:10.1371/journal.pone.0253620 · Cited by 8
“Some studies point towards reductions in temporal discounting due to pharmacological elevation of DA levels, whereas others point to an increase [18].”
BackgroundColombo, B., Iannello, P., Puglisi, G., & Antonietti, A. (2020) · Studia Psychologica · doi:10.31577/sp.2020.02.795 · Cited by 9
Lakhani, N. V., Souther, M. K., Boateng, B., & Kable, J. W. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.10.12.511959 · Cited by 9
Review: Suicide and its relationship to aggression and impulsivity
Lee, Y., Gilbert, J. R., Waldman, L. R., Zarate, C. A., & Ballard, E. D. (2025) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-025-01321-0 · Cited by 16
“This heightened activity is thought to be influenced by dopaminergic function, particularly in the PFC and ventral striatum (Joutsa et al., 2015; Pine et al., 2010).”
Chen, Y., Wang, X., Zhai, H., Zhang, Y., & Huang, J. (2021) · ACS Omega · doi:10.1021/acsomega.1c04468 · Cited by 8
Mathar, D., Wiebe, A., Tuzsus, D., Knauth, K., & Peters, J. (2023) · Psychophysiology · doi:10.1111/psyp.14381 · Cited by 9
Dopaminergic involvement in effort-based but not impulsive reward processing in smokers
Freeman, T. P., Morgan, C. J. A., Brandner, B., Almahdi, B., & Curran, H. V. (2012) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2012.10.016 · Cited by 8
Decisions under risk in Parkinson’s disease: Preserved evaluation of probability and magnitude
Sharp, M. E., Viswanathan, J., McKeown, M. J., Appel‐Cresswell, S., Stoessl, A. J., & Barton, J. J. S. (2013) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2013.08.008 · Cited by 10
Pignatti, R., Brioschi, A., Mauro, A., Zamarian, L., Wenter, J., & Semenza, C. (2012) · Neurocase · doi:10.1080/13554794.2011.633529 · Cited by 8
“In the frame of DD paradigm, a specific role for dopamine and the orbitofrontal cortex in managing impulsiveness has been clearly evidenced both in humans and animals ( Koffarnus, Newman, Grundt, Rice, & Woods, 2011 ; Peters & Buchel, 2011 ; Pine, Shiner, Seymour, & Dolan, 2010 ; Zeeb, Floresco, & Winstanley, 2010 ).”
BackgroundKalhan, S., Garrido, M. I., Hester, R., & Redish, A. D. (2023) · Neural Networks · doi:10.1016/j.neunet.2023.09.032 · Cited by 9
Controlling for temporal discounting shifts rats from geometric to human-like arithmetic bisectionPreprint
Kopec, C. D., & Brody, C. D. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/245092 · Cited by 7
“Work involving a range of species across multiple tasks has demonstrated that reward is one of the leading influences on performance during most behavioral tasks [44,51,66–68] .”
BackgroundMethylone is a rapid-acting neuroplastogen with less off-target activity than MDMA
Warner‐Schmidt, J. L., Stogniew, M., Mandell, B., Rowland, R. S., Schmidt, E. F., & Kelmendi, B. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1353131 · Cited by 6
Distinct cholinergic circuits underlie discrete effects of reward on attention
Runyon, K., Bui, T., Mazanek, S., Hartle, A. E., Marschalko, K., & Howe, W. M. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1429316 · Cited by 8
“These findings imply that output from D1 MSNs in the NAcS hyperpolarizes DA cell bodies of the VTA, an effect that should reduce action potential-dependent DA release and general behavioral impulsivity (Pine et al., 2010; Kim and Lee, 2011; Simon et al., 2013; Weiland et al., 2014).”
BackgroundDopamine and Temporal Discounting: Revisiting Pharmacology and Individual Differences
Smith, E. S., Theis, H., van Eimeren, T., Knauth, K., Tuzsus, D., Zhang, L., Mathar, D., & Peters, J. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0786-25.2025 · Cited by 6
Pharmacological Modulation of Temporal Discounting: A Systematic Review
Sarmiento, L. F., Ríos-Flórez, J. A., Ardila, H. A. P., de Sousa, P. S. L., Rosa, A. O. L., Herculano, A. M., & Gouvêia, A. (2023) · Healthcare · doi:10.3390/healthcare11071046 · Cited by 6
“[36] used the same drug, Haloperidol, where Pine et al.”
BackgroundMethodResultInfluentialIs premature ejaculation an impulse control disorder?
Özdemir, O. (2012) · Medical Hypotheses · doi:10.1016/j.mehy.2012.03.034 · Cited by 6
“Administration of the DA precursor L-DOPA increases impulsive choice in human volunteers [35].”
BackgroundDopamine increases risky choice while D2 blockade shortens decision time
Hirschbichler, S. T., Rothwell, J. C., & Manohar, S. (2022) · Experimental Brain Research · doi:10.1007/s00221-022-06501-9 · Cited by 6
“2013), other groups reported increased risk-seeking (Pine et al. 2010) but also reduced risk-seeking behaviour in participants with greater baseline impulsivity scores (Petzold et al.”
BackgroundNeural reward system reflects individual value comparison strategy in cost-benefit decisions
Corbi, Z. L. H., & Soutschek, A. (2024) · Communications Biology · doi:10.1038/s42003-024-07210-5 · Cited by 5
“…decisions as they challenge the widely held assumption that the neural reward system encodes hyperbolically discounted subjective reward values 4,14,28 , and also past pharmacological studies on the role of dopamine on intertemporal choice relied on this assumption 25,30,31 .”
Netter, P. (2021) · Neuropsychobiology · doi:10.1159/000514074 · Cited by 6
Metadata
- Authors
- Pine, A., Shiner, T., Seymour, B., & Dolan, R. J.
- Affiliations
- Wellcome Centre for Human Neuroimaging (GB)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-06-30
- Volume
- 30
- Issue
- 26
- Pages
- 8888-8896
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3059485
- OpenAlex
- W2046808635
- Cited by
- 300
- References
- 68
- Citations by year
- 2026: 7 · 2025: 16 · 2024: 13 · 2023: 14 · 2022: 19 · 2021: 15 · 2020: 18 · 2019: 16 · 2018: 14 · 2017: 17 · 2016: 22 · 2015: 18 · 2014: 19 · 2013: 27 · 2012: 30
- FWCI
- 11.78
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Max Planck Digital Library (submittedVersion, other-oa)
- Cambridge University Engineering Department Publications Database (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- Wellcome Trust (078865)
- Medical Research Council
- Economic and Social Research Council (RES-538-28-1001)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Decision Sciences › General Decision Sciences › Decision-Making and Behavioral Economics
- Keywords
- dopamine, impulsivity, delay discounting, intertemporal choice, reward value, striatum, decision-making, dopamine dysregulation syndrome, addiction, gambling addiction, attention deficit hyperactivity disorder, behavioral disinhibition, reward learning
- MeSH terms
- Adolescent, Adult, Brain, Brain Mapping, Corpus Striatum, Decision Making, Dopamine, Female, Haloperidol, Humans, Impulsive Behavior, Levodopa, Magnetic Resonance Imaging, Male, Reinforcement Schedule, Reward, Time Factors, Dopamine Agents, Dopamine Antagonists, Young Adult
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