Cited by 440Adenosine and Purinergic SignalingNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

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An update on the mechanisms of the psychostimulant effects of caffeine

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Ferré, Sergi·2008·Journal of Neurochemistry

DOI 10.1111/j.1471-4159.2007.05196.x

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Abstract

There has been a long debate about the predominant involvement of the different adenosine receptor subtypes and the preferential role of pre‐ versus post‐synaptic mechanisms in the psychostimulant effects of the adenosine receptor antagonist caffeine. Both striatal A 1 and A 2A receptors are involved in the motor‐activating and probably reinforcing effects of caffeine, although they play a different role under conditions of acute or chronic caffeine administration. The present review emphasizes the key integrative role of adenosine and adenosine receptor heteromers in the computation of information at the level of the striatal spine module (SSM). This local module is mostly represented by the dendritic spine of the medium spiny neuron with its glutamatergic and dopaminergic synapses and astroglial processes that wrap the glutamatergic synapse. In the SSM, adenosine acts both pre‐ and post‐synaptically through multiple mechanisms, which depend on heteromerization of A 1 and A 2A receptors among themselves and with D 1 and D 2 receptors, respectively. A critical aspect of the mechanisms of the psychostimulant effects of caffeine is its ability to release the pre‐ and post‐synaptic brakes that adenosine imposes on dopaminergic neurotransmission by acting on different adenosine receptor heteromers localized in different elements of the SSM.

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Background
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Background
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“Alternatively, 212 caffeine influences key neuronal signaling proteins which mediate increases in physical activity and 213 potentiates adenosine-dopamine receptor binding in striatum.(25,26) A reduced perception of effort is a 214 common response to caffeine intake, which might account for approximately 29% of its er…”
Background
Caffeine Induces a Stimulant Effect and Increases Dopamine Release in the Nucleus Accumbens Shell Through the Pulmonary Inhalation Route of Administration in Rats
Galvalisi, M., Prieto, J. P., Martinez, M. M., Abin‐Carriquiry, J. A., & Scorza, C. (2016) · Neurotoxicity Research · doi:10.1007/s12640-016-9667-8 · Cited by 29
Coffee Intake
Cornelis, M. C. (2012) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-398397-8.00012-5 · Cited by 27
Ergogenic effects of quercetin supplementation in trained rats
Casuso, R. A., Martínez‐Amat, A., López, E. J. M., Camiletti‐Moirón, D., Porres, J. M., & Aranda, P. (2013) · Journal of the International Society of Sports Nutrition · doi:10.1186/1550-2783-10-3 · Cited by 29
“A psychostimulant effect of quercetin has also been reported in vitro [8] in a manner similar to that of caffeine [9], but this effect was not found in human subjects [10].”
Background
Neuroimaging Over the Course of Parkinson's Disease: From Early Detection of the At-Risk Patient to Improving Pharmacotherapy of Later-Stage Disease
Seibyl, J. P., Russell, D., Jennings, D. L., & MAREK, K. L. (2012) · Seminars in Nuclear Medicine · doi:10.1053/j.semnuclmed.2012.06.003 · Cited by 28
Coffee and depression in Korea: the fifth Korean National Health and Nutrition Examination Survey
Park, R. J., & Moon, J.-D. (2014) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2014.247 · Cited by 28
Caffeine administration alters the behaviour and development of Galleria mellonella larvae
Maguire, R., Kunc, M., Hyršl, P., & Kavanagh, K. A. (2017) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2017.10.002 · Cited by 27
“Caffeine can also bind to intracellular calcium-channel ryanodine receptors resulting in the release of intracellular Ca2+. Caffeine can stimulate dopaminergic activity by removing the negative modulatory effects of adenosine at dopamine receptors (Ferré, 2008).”
Background
Caffeine regulates GABA transport via A1R blockade and cAMP signaling
Borges-Martins, V. P. P., Ferreira, D. D. P., Souto, A. C., Neto, J. G. O., Pereira‐Figueiredo, D., Calaza, K. D. C., Oliveira, K. J., Manhães, A. C., Reis, R. A. D. M., & Kubrusly, R. C. C. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.104550 · Cited by 27
Effect of Hibiscus syriacus Linnaeus extract and its active constituent, saponarin, in animal models of stress-induced sleep disturbances and pentobarbital-induced sleep
Kim, S., Lee, S. Y., Lee, S. M., Shim, I., & Lee, M. Y. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.112301 · Cited by 30
Acute personalized habitual caffeine doses improve attention and have selective effects when considering the fractionation of executive functions
Lanini, J., Galduróz, J. C. F., & Pompéia, S. (2015) · Human Psychopharmacology Clinical and Experimental · doi:10.1002/hup.2511 · Cited by 29
“Caffeine easily crosses the blood–brain barrier and acts mainly by blocking adenosine receptors, leading to stimulant effects (Fredholm et al., 1999; Ferre, 2008).”
Background
Neuro-Enhancement
Förstl, H. (2009) · Der Nervenarzt · doi:10.1007/s00115-009-2801-6 · Cited by 28
Can Cold Brew Coffee Be Convenient? A Pilot Study For Caffeine Content in Cold Brew Coffee Concentrate Using High Performance Liquid Chromatography
Lane, S., Palmer, J., Christie, B., Ehlting, J., & Le, C. (2017) · The Arbutus Review · doi:10.18357/tar81201716816 · Cited by 26
“This inhibition, alongside systemic vasodilation and improved calcium intake, results in a boost to physical, psychomotor, and cognitive abilities and improvements to subjective factors, such as mood and alertness (Einother & Giesbrecht, 2013; Ferré, 2008).”
Background
Methylxanthines and Drug Dependence: A Focus on Interactions with Substances of Abuse
Morelli, M., & Simola, N. (2010) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-13443-2_20 · Cited by 26
“In particular, adenosine–glutamate interactions have been suggested to participate in caffeine-elicited psychostimulation (Ferré 2008).”
Background
Caffeine Modulates Food Intake Depending on the Context That Gives Access to Food: Comparison With Dopamine Depletion
Correa, M., Miguel, N. S., López‐Cruz, L., Carratalá‐Ros, C., Olivares-García, R., & Salamone, J. D. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00411 · Cited by 26
The association between caffeine intake and testosterone: NHANES 2013–2014
Glover, F. E., Caudle, W. M., Giudice, F. D., Belladelli, F., Mulloy, E. A., Lawal, E., & Eisenberg, M. L. (2022) · Nutrition Journal · doi:10.1186/s12937-022-00783-z · Cited by 27
“Caffeine’s primary mechanism of action is antagonism of adenosine receptors, and acts on all four adenosine receptor subtypes in the brain (A1, A2a, A2b, A3) [34, 35].”
Background
Use of Stimulants to Treat Cocaine and Methamphetamine Abuse
Moeller, F., Schmitz, J. M., Herin, D., & Kjome, K. L. (2008) · Current Psychiatry Reports · doi:10.1007/s11920-008-0062-x · Cited by 27
Caffeine/sleep-deprivation interaction in mice produces complex memory effects
Onaolapo, O. J., Onaolapo, A. Y., Akanmu, M. A., & Olayiwola, G. (2015) · Annals of Neurosciences · doi:10.5214/ans.0972.7531.220304 · Cited by 26
Caffeine alleviates progressive motor deficits in a transgenic mouse model of spinocerebellar ataxia
Gonçalves, N., Simões, A., Prediger, R., Hirai, H., Cunha, R., & de Almeida, L. P. (2017) · Annals of Neurology · doi:10.1002/ana.24867 · Cited by 31
A Survey of Energy Drink Consumption Patterns Among College Students at a Mostly Hispanic University
Cabezas-Bou, E., León-Arbucias, J. D., Matos-Vergara, N., Álvarez-Bagnarol, Y., Ortega-Guzmán, J., Narváez-Pérez, K., Cruz‐Bermúdez, N. D., & Díaz‐Ríos, M. (2016) · Journal of Caffeine Research · doi:10.1089/jcr.2016.0011 · Cited by 25
Coffee time: Low caffeine dose promotes attention and focus in zebrafish
Ruiz-Oliveira, J., Silva, P. F., & Luchiari, A. C. (2019) · Learning & Behavior · doi:10.3758/s13420-018-0369-3 · Cited by 25
“Associative learning Caffeine is one of the most consumed stimulants in the world (Ferré, 2008; Lieberman, 1992).”
Background
The Use of Caffeine by People with Epilepsy: the Myths and the Evidence
Bauer, P. R., & Sander, J. W. A. S. (2019) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-019-0948-5 · Cited by 25
Purinergic transmission in depressive disorders
Szopa, A., Socała, K., Serefko, A., Doboszewska, U., Wróbel, A., Poleszak, E., & Właź, P. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107821 · Cited by 25
Evaluation of the Anxiolytic and Antidepressant Activities of the Aqueous Extract fromCamellia euphlebiaMerr. ex Sealy in Mice
He, D., Wang, X., Zhang, P., Luo, X., Li, X., Wang, L., Li, S., & Xu, Y. (2015) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2015/618409 · Cited by 26
“In particular, antagonism of A2A receptors increases neurotransmission through dopamine D2 receptors, and antagonism of A1 receptors interacts with D1 receptors and regulates the release of neurotransmitters such as dopamine, glutamate, and acetylcholine [37, 38].”
Background
The heat is on: thermodynamic analysis in fragment-based drug discovery
Edink, E., Jansen, C., Leurs, R., & de Esch, I. J. P. (2010) · Drug Discovery Today Technologies · doi:10.1016/j.ddtec.2010.12.001 · Cited by 25
Acute and adaptive motor responses to caffeine in adolescent and adult rats
Rhoads, D. E., Huggler, A. L., & Rhoads, L. J. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.04.001 · Cited by 24
Functional roles of ST8SIA3-mediated sialylation of striatal dopamine D2 and adenosine A2A receptors
Lin, C., Lai, H., Chen, H., Siew, J. J., Hsiao, C.-T., Chang, H.-C., Liao, K., Tsai, S.-C., Wu, C., Kitajima, K., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0529-z · Cited by 25
Caffeine Timing Improves Lower-Body Muscular Performance: A Randomized Trial
Harty, P. S., Zabriskie, H. A., Stecker, R. A., Currier, B. S., Tinsley, G. M., Surowiec, K., Jagim, A. R., Richmond, S. R., & Kerksick, C. M. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2020.585900 · Cited by 31
“The ergogenic effects of caffeine have largely been attributed to its function as an adenosine receptor antagonist (4), as consumption has been shown to increase motor activity, neuromuscular coordination, and physiological arousal (5, 6).”
Background
Brain activity during a working memory task after daily caffeine intake and caffeine withdrawal: a randomized double-blind placebo-controlled trial
Lin, Y.-S., Weibel, J., Landolt, H., Santini, F., Slawik, H. C., Borgwardt, S., Cajochen, C., & Reichert, C. (2023) · Scientific Reports · doi:10.1038/s41598-022-26808-5 · Cited by 33
Relationship between daily coffee intake and suicidal ideation
Park, H., Suh, B. S., & Lee, K. (2019) · Journal of Affective Disorders · doi:10.1016/j.jad.2019.06.023 · Cited by 24
Maximising Recovery of Bioactive Compounds from Coffee Pulp Waste Using Microwave-assisted Extraction
Tran, T. M. K., Akanbi, T. O., Kirkman, T., Nguyen, M. H., & Vuong, Q. V. (2022) · European Journal of Engineering and Technology Research · doi:10.24018/ejeng.2022.7.3.2812 · Cited by 24
“Caffeine is a kind of alkaloid named 1,3,7-trimethylxanthine [11]; it produces arasoul effects, stimulates nervous activity [12] and improves metabolic system [11].”
Background
Effect of Pre-Exercise Caffeine Intake on Endurance Performance and Core Temperature Regulation During Exercise in the Heat: A Systematic Review with Meta-Analysis
Naulleau, C., Jeker, D., Pancrate, T., Claveau, P., Deshayes, T. A., Burke, L. M., & Goulet, E. D. B. (2022) · Sports Medicine · doi:10.1007/s40279-022-01692-1 · Cited by 24
“Indeed, caffeine enhances dopamine signaling in the brain [60] through its effect on adenosine receptors [61, 62].”
Background
Caffeine's Implications for Women's Health and Survey of Obstetrician-Gynecologists' Caffeine Knowledge and Assessment Practices
Anderson, B. L., Juliano, L. M., & Schulkin, J. A. (2009) · Journal of Women s Health · doi:10.1089/jwh.2008.1186 · Cited by 23
“receptors.(4) It produces positive subjective effects (e.”
Acute effects of caffeine on threat-selective attention: moderation by anxiety and EEG theta/beta ratio
Son, D. V., Schalbroeck, R., Angelidis, A., van der Wee, N. J. A., van der Does, W. A. J., & Putman, P. (2018) · Biological Psychology · doi:10.1016/j.biopsycho.2018.05.006 · Cited by 25
“…explanation of the beta decrease found in the current study might be because participants had to sit still during the eight-minute baseline measurement even though the caffeine manipulation might have caused motoric stimulation (Fisone, Borgkvist & Usiello, 2004; for a review see Ferré, 2008).”
Result
The Relationship Between Cognition and Cerebrovascular Reactivity: Implications for Task-Based fMRI
Williams, R. J., MacDonald, M. E., Mazerolle, E. L., & Pike, G. B. (2021) · Frontiers in Physics · doi:10.3389/fphy.2021.645249 · Cited by 23
“By blocking the action of inhibitory neurotransmitter adenosine on these receptors, caffeine produces a stimulation effect through disinhibition [170].”
Background
Theanine maintains sleep quality in healthy young women by suppressing the increase in caffeine-induced wakefulness after sleep onset
Baba, Y., Takihara, T., & Okamura, N. (2023) · Food & Function · doi:10.1039/d3fo01247f · Cited by 22
Caffeine intake modulates the functioning of the attentional networks depending on consumption habits and acute exercise demands
Huertas, F., Blasco, E., Moratal, C., & Lupiáñez, J. (2019) · Scientific Reports · doi:10.1038/s41598-019-46524-x · Cited by 23
Dose-dependent neuroprotective effect of caffeine on a rotenone-induced rat model of parkinsonism: A histological study
Soliman, A. M., Fathalla, A., & Moustafa, A. A. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.04.057 · Cited by 22
Individual differences in the energizing effects of caffeine on effort-based decision-making tests in rats
Miguel, N. S., Pardo, M., Carratalá‐Ros, C., López‐Cruz, L., Salamone, J. D., & Correa, M. (2018) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2018.04.004 · Cited by 24
“Nacb has also a high concentration of adenosine A1 and A2A receptors, (Ferré, 1997, 2008; Ferré et al., 1997, 2005; Fuxe et al., 2003).”
Energy- Drinks: Composition and Health Benefits
Yunusa, I. U., & Ahmad, I. (2012) · Bayero Journal of Pure and Applied Sciences · doi:10.4314/bajopas.v4i2.38 · Cited by 29
“The blockage of adenosine to the neurons causes the sleep promoting effects of adenosine to stop, resulting in the neurons speeding up instead of slowing down (Ferre, 2008).”
Background
Spatial Regulation Control of Oxygen Metabolic Consumption in Mouse Brain
Zhou, L., Li, X., & Su, B. (2022) · Advanced Science · doi:10.1002/advs.202204468 · Cited by 22
Caffeine, D-glucuronolactone and Taurine Content in Energy Drinks: Exposure and Risk Assessment
Rubio, C., Cámara, M., Giner, R. M., González‐Muñoz, M. J., López‐García, E., Morales, F. J., Moreno-Arribas, M. V., Portillo, M. P., & Bethencourt-Barbuzano, E. (2022) · Nutrients · doi:10.3390/nu14235103 · Cited by 21
Effects of oral caffeine administration to sows with induced parturition on hypoxia in piglets
Superchi, P., Mazzoni, C., Zanardelli, P., Piancastelli, C., Zambini, E. M., Beretti, V., & Sabbioni, A. (2013) · Livestock Science · doi:10.1016/j.livsci.2013.08.003 · Cited by 21
“Caffeine in addition to exercising psychostimulant effects (Ferré, 2008), acts on brainstem respiratory structures stimulating the medullar respiratory center, increasing sensitivity to carbon dioxide, and improving diaphragmatic contractility (Orozco-Gregorio et al.”
Background
Effects of oral administration of caffeine on some physiological parameters and maternal behaviour of sows at farrowing
Superchi, P., Saleri, R., Farina, E., Cavalli, V., Riccardi, E., & Sabbioni, A. (2016) · Research in Veterinary Science · doi:10.1016/j.rvsc.2016.01.023 · Cited by 21
Modulatory effects of caffeine on oxidative stress and anxiety-like behavior in ovariectomized rats
Caravan, I., Sevastre-Berghian, A., Moldovan, R., Decea, N., Orăsan, R., & Filip, G. A. (2016) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2015-0502 · Cited by 20
“caffeine, the increased expression of A1 ARs may lead to a shift in the A1/A2A ARs balance (Ferré 2008; Shi et al. 1993).”
Background
Well-Known Antioxidants and Newcomers in Sport Nutrition
Belviranlı, M., & Okudan, N. (2014) · CRC Press eBooks · doi:10.1201/b17442-5 · Cited by 20
Evaluating the Validity of Caffeine Use Disorder
Budney, A. J., Lee, D. C., & Juliano, L. M. (2015) · Current Psychiatry Reports · doi:10.1007/s11920-015-0611-z · Cited by 22

Authors: Ferré, S.
Affiliations: National Institutes of Health (US)
Corresponding author: Ferré, Sergi
ORCID: Ferré, Sergi
Venue: Journal of Neurochemistry
Publisher: Wiley
Published: 2007-12-18
Volume: 105
Issue: 4
Pages: 1067-1079
ISSN: 0022-3042 (ISSN-L)
1471-4159
DOI: 10.1111/j.1471-4159.2007.05196.x
OpenAlex: W1994970739
Cited by: 440
References: 129
Citations by year: 2026: 12 · 2025: 19 · 2024: 14 · 2023: 23 · 2022: 31 · 2021: 30 · 2020: 15 · 2019: 26 · 2018: 24 · 2017: 18 · 2016: 32 · 2015: 32 · 2014: 25 · 2013: 34 · 2012: 29
FWCI: 1.52
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Journal of Neurochemistry (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute on Drug Abuse
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Adenosine and Purinergic Signaling
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: caffeine, psychostimulant effects, adenosine receptors, adenosine A1 receptor, adenosine A2A receptor, receptor heteromers, dopamine signaling, glutamatergic synapses, dopamine D1 receptor, dopamine D2 receptor, motor activation, reinforcement, adenosine
MeSH terms: Adenosine, Central Nervous System Stimulants, Animals, Caffeine, Humans, Receptors, Purinergic P1, Purinergic P1 Receptor Agonists

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An update on the mechanisms of the psychostimulant effects of caffeine

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