Dopamine, effort-based choice, and behavioral economics: basic and translational research.

Salamone, John D.; Correa, Merce; Yang, Jen-Hau; Rotolo, Renee; Presby, Rose

doi:10.3389/fnbeh.2018.00052

Cited by 142Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesDecision-Making and Behavioral Economics

Dopamine, effort-based choice, and behavioral economics: basic and translational research.

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Salamone, John D., Correa, Merce, Yang, Jen-Hau, Rotolo, Renee, Presby, Rose·2018·Frontiers in Behavioral Neuroscience

DOI 10.3389/fnbeh.2018.00052PMC PMC5876251

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Abstract

Operant behavior is not only regulated by factors related to the quality or quantity of reinforcement, but also by the work requirements inherent in performing instrumental actions. Moreover, organisms often make effort-related decisions involving economic choices such as cost/benefit analyses. Effort-based decision making is studied using behavioral procedures that offer choices between high-effort options leading to relatively preferred reinforcers vs. low effort/low reward choices. Several neural systems, including the mesolimbic dopamine (DA) system and other brain circuits, are involved in regulating effort-related aspects of motivation. Considerable evidence indicates that mesolimbic DA transmission exerts a bi-directional control over exertion of effort on instrumental behavior tasks. Interference with DA transmission produces a low-effort bias in animals tested on effort-based choice tasks, while increasing DA transmission with drugs such as DA transport blockers tends to enhance selection of high-effort options. The results from these pharmacology studies are corroborated by the findings from recent articles using optogenetic, chemogenetic and physiological techniques. In addition to providing important information about the neural regulation of motivated behavior, effort-based choice tasks are useful for developing animal models of some of the motivational symptoms that are seen in people with various psychiatric and neurological disorders (e.g., depression, schizophrenia, Parkinson's disease). Studies of effort-based decision making may ultimately contribute to the development of novel drug treatments for motivational dysfunction.

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Incentive salience is often a spur to action, reflecting the overlap between dopamine functions of motivation and of movement.
“Incentive salience is often thus a spur to action, reflecting the overlap between dopamine functions of motivation and of movement (Salamone et al., 2015, 2018).”
From Evolving Concepts of Emotion and Motivation (2018) · cites this paper as Salamone et al., 2018

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The adenosine A2A antagonist MSX-3 reverses the effects of the dopamine antagonist haloperidol on effort-related decision making in a T-maze cost/benefit procedure
Mott, A. M., Nunes, E. J., Collins, L. E., Port, R. G., Sink, K. S., Hockemeyer, J., Müller, C. E., & Salamone, J. D. (2009) · Psychopharmacology · doi:10.1007/s00213-008-1441-z · Cited by 116 · see citing works
Cannabinoid CB1 antagonists and dopamine antagonists produce different effects on a task involving response allocation and effort-related choice in food-seeking behavior
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The VMAT-2 Inhibitor Tetrabenazine Affects Effort-Related Decision Making in a Progressive Ratio/Chow Feeding Choice Task: Reversal with Antidepressant Drugs
Randall, P. A., Lee, C. A., Nunes, E. J., Yohn, S. E., Nowak, V., Khan, B., Shah, P., Pandit, S., Vemuri, K. V., Makriyannis, A., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099320 · Cited by 112 · see citing works
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Nunes, E. J., Randall, P. A., Estrada, A., Epling, B. P., Hart, E. E., Lee, C. A., Baqi, Y., Müller, C. E., Correa, M., & Salamone, J. D. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3285-4 · Cited by 108 · see citing works
A microdialysis study of nucleus accumbens core and shell dopamine during operant responding in the rat
Sokolowski, J. D., Conlan, A., & Salamone, J. D. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00066-9 · Cited by 108 · see citing works
Motivational states influence effort-based decision making in rats: The role of dopamine in the nucleus accumbens
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Decreasing Striatopallidal Pathway Function Enhances Motivation by Energizing the Initiation of Goal-Directed Action
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Nucleus Accumbens Dopamine and the Forebrain Circuitry Involved in Behavioral Activation and Effort-Related Decision Making: Implications for Understanding Anergia and Psychomotor Slowing in Depression
Salamone, J. D., Correa, M., Mingote, S., Weber, S. M., & Farrar, A. M. (2006) · Current Psychiatry Reviews · doi:10.2174/157340006776875914 · Cited by 104 · see citing works
Forebrain circuitry involved in effort-related choice: Injections of the GABAA agonist muscimol into ventral pallidum alter response allocation in food-seeking behavior
Farrar, A. M., Font, L., Pereira, M., Mingote, S., Bunce, J. G., Chrobak, J. J., & Salamone, J. D. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2007.12.034 · Cited by 103 · see citing works
Intra-accumbens injections of the adenosine A2A agonist CGS 21680 affect effort-related choice behavior in rats
Font, L., Mingote, S., Farrar, A. M., Pereira, M., Worden, L. T., Stopper, C. M., Port, R. G., & Salamone, J. D. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1174-z · Cited by 102 · see citing works
Perturbations in Effort-Related Decision-Making Driven by Acute Stress and Corticotropin-Releasing Factor
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Effects of bupropion on simulated demand for cigarettes and the subjective effects of smoking
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The role of dopamine D1 receptor transmission in effort-related choice behavior: Effects of D1 agonists
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The VMAT-2 inhibitor tetrabenazine alters effort-related decision making as measured by the T-maze barrier choice task: reversal with the adenosine A2A antagonist MSX-3 and the catecholamine uptake blocker bupropion
Yohn, S. E., Thompson, C., Randall, P. A., Lee, C. A., Müller, C. E., Baqi, Y., Correa, M., & Salamone, J. D. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3766-0 · Cited by 97 · see citing works
Associations between the effort-reward imbalance model of workplace stress and indices of cardiovascular health: a systematic review and meta-analysis
Eddy, P., Wertheim, E. H., Kingsley, M., & Wright, B. J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.10.025 · Cited by 96 · cited 1× · see citing works
“Within the fields of industrial/organizational psychology and behavioral health, it is becoming more and more emphasized that effort/reward trade-offs can be a substantial source of stress in the workplace (Eddy et al., 2017, 2018).”
Background
Dissociation of the role of nucleus accumbens dopamine in responding to reward-predictive cues and waiting for reward
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Measuring reinforcement learning and motivation constructs in experimental animals: Relevance to the negative symptoms of schizophrenia
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Effort-related motivational effects of the pro-inflammatory cytokine interleukin-6: pharmacological and neurochemical characterization
Yohn, S. E., Arif, Y., Haley, A., Tripodi, G., Baqi, Y., Müller, C. E., Miguel, N. S., Correa, M., & Salamone, J. D. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4392-9 · Cited by 93 · see citing works
Toward a generalizable model of symptoms in major depressive disorder
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Tetrabenazine is neuroprotective in Huntington's disease mice
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Reinforcer Magnitude and Progressive Ratio Responding in the Rat: Effects of Increased Effort, Prefeeding, and Extinction
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Nucleus Accumbens Dopamine Depletions and Time-Constrained Progressive Ratio Performance
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Physical and cognitive effort discounting across different reward magnitudes: Tests of discounting models
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Not All Antidepressants Are Created Equal: Differential Effects of Monoamine Uptake Inhibitors on Effort-Related Choice Behavior
Yohn, S. E., Collins, S. L., Contreras-Mora, H. M., Errante, E. L., Rowland, M. A., Correa, M., & Salamone, J. D. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.188 · Cited by 81 · see citing works
The hippocampus and reward: Effects of hippocampal lesions on progressive-ratio responding.
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Neurobiological basis of motivational deficits in psychopathology
Salamone, J. D., Koychev, I. G., Correa, M., & McGuire, P. K. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2014.08.014 · Cited by 80 · see citing works
The dopamine reuptake inhibitor MRZ-9547 increases progressive ratio responding in rats
Sommer, S., Danysz, W., Russ, H., Valastro, B., Flik, G., & Hauber, W. (2014) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145714000996 · Cited by 80 · see citing works
The adenosine A2A antagonist MSX-3 reverses the effort-related effects of dopamine blockade: differential interaction with D1 and D2 family antagonists
Worden, L. T., Shahriari, M., Farrar, A. M., Sink, K. S., Hockemeyer, J., Müller, C. E., & Salamone, J. D. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1396-0 · Cited by 79 · see citing works
Dopamine Manipulation Affects Response Vigor Independently of Opportunity Cost
Zénon, A., Devesse, S., & Olivier, E. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4467-15.2016 · Cited by 79 · see citing works
Resolution of sleepiness and fatigue: A comparison of bupropion and selective serotonin reuptake inhibitors in subjects with major depressive disorder achieving remission at doses approved in the European Union
Cooper, J. A., Tucker, V. L., & Papakostas, G. I. (2013) · Journal of Psychopharmacology · doi:10.1177/0269881113514878 · Cited by 77 · see citing works
Blockade of uptake for dopamine, but not norepinephrine or 5-HT, increases selection of high effort instrumental activity: Implications for treatment of effort-related motivational symptoms in psychopathology
Yohn, S. E., Errante, E. L., Rosenbloom-Snow, A., Somerville, M., Rowland, M. A., Tokarski, K., Zafar, N., Correa, M., & Salamone, J. D. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.06.018 · Cited by 76 · see citing works
Effects of lisdexamfetamine and s-citalopram, alone and in combination, on effort-related choice behavior in the rat
Yohn, S. E., López‐Cruz, L., Hutson, P. H., Correa, M., & Salamone, J. D. (2015) · Psychopharmacology · doi:10.1007/s00213-015-4176-7 · Cited by 74 · see citing works
Acute phenylalanine/tyrosine depletion reduces motivation to smoke cigarettes across stages of addiction
Venugopalan, V. V., Casey, K. F., O'Hara, C., O'Loughlin, J., Benkelfat, C., Fellows, L. K., & Leyton, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.135 · Cited by 70 · see citing works
Phasic Dopamine Transmission Reflects Initiation Vigor and Exerted Effort in an Action- and Region-Specific Manner
Ko, D., & Wanat, M. J. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1279-15.2016 · Cited by 70 · see citing works
The relationship between sexual functioning among couples undergoing infertility treatment: a pair of perfect gloves
Yeoh, S. H., Razali, R., Sidi, H., Razi, Z. R. M., Midin, M., Jaafar, N. R. N., & Das, S. (2012) · Comprehensive Psychiatry · doi:10.1016/j.comppsych.2012.09.002 · Cited by 67 · see citing works
Selection of sucrose concentration depends on the effort required to obtain it: studies using tetrabenazine, D1, D2, and D3 receptor antagonists
Pardo, M., López‐Cruz, L., Miguel, N. S., Salamone, J. D., & Correa, M. (2015) · Psychopharmacology · doi:10.1007/s00213-015-3872-7 · Cited by 66 · see citing works
Schizophrenia in Translation: Dissecting Motivation in Schizophrenia and Rodents
Simpson, E. H., Waltz, J. A., Kellendonk, C., & Balsam, P. D. (2012) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs114 · Cited by 65 · see citing works
The relationship between change in apathy and changes in cognition and functional outcomes in currently non-depressed SSRI-treated patients with major depressive disorder
Rothschild, A. J., Raskin, J., Wang, C.-N., Marangell, L. B., & Fava, M. (2014) · Comprehensive Psychiatry · doi:10.1016/j.comppsych.2013.08.008 · Cited by 59 · see citing works
Progressive reinforcement schedules: A review and evaluation
Stewart, W. J. (1975) · Australian Journal of Psychology · doi:10.1080/00049537508255235 · Cited by 56 · see citing works
Rats assess costs and benefits according to an internal standard
VANDENBOS, R., VANDERHARST, J., Jonkman, S., Schilders, M., & Spruijt, B. M. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.03.035 · Cited by 53 · see citing works
Reassessing wanting and liking in the study of mesolimbic influence on food intake
Nicola, S. M. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00234.2016 · Cited by 50 · see citing works
Enhancing excitability of dopamine neurons promotes motivational behaviour through increased action initiation
Boekhoudt, L., Wijbrans, E. C., Man, J. H. K., Luijendijk, M. C. M., de Jong, J. W., Plasse, G., Vanderschuren, L. J. M. J., & Adan, R. A. H. (2017) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2017.11.005 · Cited by 49 · see citing works
Predicting Motivation: Computational Models of PFC Can Explain Neural Coding of Motivation and Effort-based Decision-making in Health and Disease
Vassena, E., Deraeve, J., & Alexander, W. H. (2017) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01160 · Cited by 46 · see citing works
DEPRES II (Depression Research in European Society II)
Tylee, A. T., Gastpar, M., Lépine, J., & Mendlewicz, J. (1999) · International Clinical Psychopharmacology · doi:10.1097/00004850-199905030-00001 · Cited by 46 · see citing works
Psychostimulants in the therapy of treatment-resistant depression: review of the literature and findings from a retrospective study in 65 depressed patients
Stotz, G., Woggon, B., & Angst, J. (1999) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.1999.1.3/gstotz · Cited by 45 · see citing works
Evaluation of the effort-related motivational effects of the novel dopamine uptake inhibitor PRX-14040
Yohn, S. E., Gogoj, A., Haque, A. F., López‐Cruz, L., Haley, A., Huxley, P., Baskin, P. P., Correa, M., & Salamone, J. D. (2016) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2016.06.004 · Cited by 45 · see citing works
Slow phasic changes in nucleus accumbens dopamine release during fixed ratio acquisition: a microdialysis study
Segovia, K. N., Correa, M., & Salamone, J. D. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.07.078 · Cited by 44 · see citing works
Inhibiting Mesolimbic Dopamine Neurons Reduces the Initiation and Maintenance of Instrumental Responding
Fischbach-Weiss, S., Reese, R. M., & Janak, P. H. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.12.003 · Cited by 44 · see citing works
Anterior cingulate cortex supports effort allocation towards a qualitatively preferred option
Hart, E. E., Gerson, J. O., Zoken, Y., Garcia, M., & Izquierdo, A. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13608 · Cited by 41 · see citing works
Quantifying Reinforcement Value and Demand for Psychoactive Substances in Humans
Heinz, A. J., Lilje, T. C., Kassel, J. D., & de Wit, H. (2012) · Current Drug Abuse Reviews · doi:10.2174/1874473711205040002 · Cited by 40 · see citing works
Pharmacological stimuli decreasing nucleus accumbens dopamine can act as positive reinforcers but have a low addictive potential
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Changes in nucleus accumbens and neostriatal c‐Fos and DARPP‐32 immunoreactivity during different stages of food‐reinforced instrumental training
Segovia, K. N., Correa, M., Lennington, J. B., Conover, J. C., & Salamone, J. D. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08036.x · Cited by 40 · see citing works
Role of dopamine–adenosine interactions in the brain circuitry regulating effort-related decision making: insights into pathological aspects of motivation
Salamone, J. D., Correa, M., Farrar, A. M., Nunes, E. J., & Collins, L. E. (2010) · Future Neurology · doi:10.2217/fnl.10.19 · Cited by 40 · see citing works
Orbitofrontal cortex and basolateral amygdala lesions result in suboptimal and dissociable reward choices on cue-guided effort in rats.
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Disruptions in effort-based decision-making and consummatory behavior following antagonism of the dopamine D2 receptor
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Behavioral activation, effort-based choice, and elasticity of demand for motivational stimuli: Basic and translational neuroscience approaches.
Salamone, J. D., Correa, M., Yohn, S. E., Yang, J.-H., Somerville, M., Rotolo, R. A., & Presby, R. E. (2017) · Motivation Science · doi:10.1037/mot0000070 · Cited by 35 · see citing works
An economic approach to animal models of alcoholism.
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TESTS OF BEHAVIORAL‐ECONOMIC ASSESSMENTS OF RELATIVE REINFORCER EFFICACY II: ECONOMIC COMPLEMENTS
Madden, G. J., Smethells, J. R., Ewan, E. E., & Hursh, S. R. (2007) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.2007.88-355 · Cited by 29 · see citing works
Genetic inhibition of neurotransmission reveals role of glutamatergic input to dopamine neurons in high-effort behavior
Hutchison, M. A., Gu, X., Adrover, M. F., LEE, M. R., Hnasko, T. S., Alvarez, V. A., & Lü, W. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.7 · Cited by 29 · see citing works
The Effects of Traditional Tonics on Fatigue in Mice Differ from Those of the Antidepressant Imipramine: A Pharmacological and Behavioral Study
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Modafinil Augmentation for Residual Symptoms of Fatigue in Patients with a Partial Response to Antidepressants
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Dopamine D2-Like Receptors and Behavioral Economics of Food Reinforcement
Soto, P. L., Hiranita, T., Xu, M., Hursh, S. R., Grandy, D. K., & Katz, J. L. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.223 · Cited by 21 · see citing works
Basolateral amygdala supports the maintenance of value and effortful choice of a preferred option
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Comparison of the reinforcing efficacy of two dopamine D2-like receptor agonists in rhesus monkeys using a progressive-ratio schedule of reinforcement
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Networks of VTA Neurons Encode Real-Time Information about Uncertain Numbers of Actions Executed to Earn a Reward
Wood, J. T., Simon, N. W., Koerner, F. S., Kass, R. E., & Moghaddam, B. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00140 · Cited by 17 · see citing works
Economic Concepts in the Behavioral Study of Addiction
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Steep effort discounting of a preferred reward over a freely-available option in prolonged methamphetamine withdrawal in male rats
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Oral Ingestion and Intraventricular Injection of Curcumin Attenuates the Effort-Related Effects of the VMAT-2 Inhibitor Tetrabenazine: Implications for Motivational Symptoms of Depression
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Mind Your Grip: Even Usual Dexterous Manipulation Requires High Level Cognition
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Assessment of a glycine uptake inhibitor in animal models of effort-related choice behavior: implications for motivational dysfunctions
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Neural Correlates of Impaired Reward–Effort Integration in Remitted Bulimia Nervosa
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Networks of VTA neurons encode real-time information about uncertain numbers of actions executed to earn a rewardPreprint
Wood, J. T., Simon, N. W., Koerner, S., et al. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/084970 · Cited by 2 · see citing works

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Evolving Concepts of Emotion and Motivation
Berridge, K. C. (2018) · Frontiers in Psychology · doi:10.3389/fpsyg.2018.01647 · Cited by 273 · see citing works
Affective valence in the brain: modules or modes?
Berridge, K. C. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0122-8 · Cited by 183 · see citing works
The neural basis of effort valuation: A meta-analysis of functional magnetic resonance imaging studies
Lopez-Gamundi, P., Yao, Y., Chong, T. T. ‐., Heekeren, H. R., Herrero, E. M., & Marco‐Pallarés, J. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.10.024 · Cited by 116 · see citing works
A Reward-Based Framework of Perceived Control
Ly, V., Wang, K. S., Bhanji, J. P., & Delgado, M. R. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00065 · Cited by 112 · see citing works
Separate gut-brain circuits for fat and sugar reinforcement combine to promote overeating
McDougle, M. J., de Araujo, A., Singh, A., Yang, M., Braga, I., Paillé, V., Méndez‐Hernández, R., Vergara, M., Woodie, L. N., Gour, A., et al. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2023.12.014 · Cited by 106 · see citing works
Animal models of depression: pros and cons
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Authors: Salamone, J. D., Correa, M., Yang, J.-H., Rotolo, R., & Presby, R.
Affiliations: University of Connecticut (US)
Corresponding author: Salamone, John D.
ORCID: Salamone, John D.
Rotolo, Renee
Presby, Rose
Venue: Frontiers in Behavioral Neuroscience
Publisher: Frontiers Media SA
Published: 2018-03-23
Volume: 12
Pages: 52-52
ISSN: 1662-5153 (ISSN-L)
DOI: 10.3389/fnbeh.2018.00052
PMC: PMC5876251
OpenAlex: W2790892419
Cited by: 142
References: 157
Citations by year: 2026: 14 · 2025: 14 · 2024: 16 · 2023: 14 · 2022: 17 · 2021: 19 · 2020: 21 · 2019: 14 · 2018: 13
FWCI: 2.17
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Repositori UJI (Universitat Jaume I) (publishedVersion, cc-by-sa)
LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-sa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: National Institutes of Health
National Institute of Mental Health (R03MH112984)
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, effort-based decision making, mesolimbic dopamine system, cost-benefit analysis, instrumental behavior, motivation, optogenetics, chemogenetics, depression, schizophrenia, Parkinson's disease

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