Skip to main content
SpringerLink
Log in

Adenosine signaling in striatal circuits and alcohol use disorders

  • Minireview
  • Published:
Molecules and Cells

Abstract

Adenosine signaling has been implicated in the pathophysiology of alcohol use disorders and other psychiatric disorders such as anxiety and depression. Numerous studies have indicated a role for A1 receptors (A1R) in acute ethanol-induced motor incoordination, while A2A receptors (A2AR) mainly regulate the rewarding effect of ethanol in mice. Recent findings have demonstrated that dampened A2AR-mediated signaling in the dorsomedial striatum (DMS) promotes ethanol-seeking behaviors. Moreover, decreased A2AR function is associated with decreased CREB activity in the DMS, which enhances goal-oriented behaviors and contributes to excessive ethanol drinking in mice. Interestingly, caffeine, the most commonly used psychoactive substance, is known to inhibit both the A1R and A2AR. This dampened adenosine receptor function may mask some of the acute intoxicating effects of ethanol. Furthermore, based on the fact that A2AR activity plays a role in goal-directed behavior, caffeine may also promote ethanol-seeking behavior. The A2AR is enriched in the striatum and exclusively expressed in striatopallidal neurons, which may be responsible for the regulation of inhibitory behavioral control over drug rewarding processes through the indirect pathway of the basal ganglia circuit. Furthermore, the antagonistic interactions between adenosine and dopamine receptors in the striatum also play an integral role in alcoholism and addiction-related disorders. This review focuses on regulation of adenosine signaling in striatal circuits and the possible implication of caffeine in goal-directed behaviors and addiction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arolfo, M.P., Yao, L., Gordon, A.S., Diamond, I., and Janak, P.H. (2004). Ethanol operant self-administration in rats is regulated by adenosine A2 receptors. Alcohol. Clin. Exp. Res. 28, 1308–1316.

    Article  PubMed  CAS  Google Scholar 

  • Asatryan, L., Nam, H.W., Lee, M.R., Thakkar, M.M., Dar, M.S., Davies, D.L., and Choi, D.S. (2011). Implication of the Purinergic System in Alcohol Use Disorders. Alcohol. Clin. Exp. Res. 35, 584–594.

    Article  PubMed  CAS  Google Scholar 

  • Baldwin, S.A., Mackey, J.R., Cass, C.E., and Young, J.D. (1999). Nucleoside transporters: molecular biology and implications for therapeutic development. Mol. Med. Today 5, 216–224.

    Article  PubMed  CAS  Google Scholar 

  • Baldwin, S.A., Beal, P.R., Yao, S.Y., King, A.E., Cass, C.E., and Young, J.D. (2004). The equilibrative nucleoside transporter family, SLC29. Pflugers Arch. 447, 735–743.

    Article  PubMed  CAS  Google Scholar 

  • Baldwin, S.A., Yao, S.Y., Hyde, R.J., Ng, A.M., Foppolo, S., Barnes, K., Ritzel, M.W., Cass, C.E., and Young, J.D. (2005). Functional characterisation of novel human and mouse equilibrative nucleoside transporters (hENT3 and mENT3) located in intracellular membranes. J. Biol. Chem. 280, 15880–15887.

    Article  PubMed  CAS  Google Scholar 

  • Balleine, B.W., Delgado, M.R., and Hikosaka, O. (2007). The role of the dorsal striatum in reward and decision-making. J. Neurosci. 27, 8161–8165.

    Article  PubMed  CAS  Google Scholar 

  • Brundege, J.M., Diao, L., Proctor, W.R., and Dunwiddie, T.V. (1997). The role of cyclic AMP as a precursor of extracellular adenosine in the rat hippocampus. Neuropharmacology 36, 1201–1210.

    Article  PubMed  CAS  Google Scholar 

  • Butler, T.R., and Prendergast, M.A. (2012). Neuroadaptations in adenosine receptor signaling following long-term ethanol exposure and withdrawal. Alcohol. Clin. Exp. Res. 36, 4–13.

    Article  PubMed  CAS  Google Scholar 

  • Chen, J.F., Huang, Z., Ma, J., Zhu, J., Moratalla, R., Standaert, D., Moskowitz, M.A., Fink, J.S., and Schwarzschild, M.A. (1999). A(2A) adenosine receptor deficiency attenuates brain injury induced by transient focal ischemia in mice. J. Neurosci. 19, 9192–9200.

    PubMed  CAS  Google Scholar 

  • Chen, J.F., Moratalla, R., Impagnatiello, F., Grandy, D.K., Cuellar, B., Rubinstein, M., Beilstein, M.A., Hackett, E., Fink, J.S., Low, M.J., et al. (2001). The role of the D(2) dopamine receptor (D(2)R) in A(2A) adenosine receptor (A(2A)R)-mediated behavioral and cellular responses as revealed by A(2A) and D(2) receptor knockout mice. Proc. Natl. Acad. Sci. USA 98, 1970–1975.

    Article  PubMed  CAS  Google Scholar 

  • Chen, J., Nam, H.W., Lee, M.R., Hinton, D.J., Choi, S., Kim, T., Kawamura, T., Janak, P.H., and Choi, D.-S. (2010). Altered glutamatergic neurotransmission in the striatum regulates ethanol sensitivity and intake in mice lacking ENT1. Behav. Brain Res. 208, 636–642.

    Article  PubMed  CAS  Google Scholar 

  • Choi, D.S., Cascini, M.G., Mailliard, W., Young, H., Paredes, P., McMahon, T., Diamond, I., Bonci, A., and Messing, R.O. (2004). The type 1 equilibrative nucleoside transporter regulates ethanol intoxication and preference. Nat. Neurosci. 7, 855–861.

    Article  PubMed  CAS  Google Scholar 

  • Ciruela, F., Casado, V., Rodrigues, R.J., Lujan, R., Burgueno, J., Canals, M., Borycz, J., Rebola, N., Goldberg, S.R., Mallol, J., et al. (2006a). Presynaptic control of striatal glutamatergic neurotransmission by adenosine A1-A2A receptor heteromers. J. Neurosci. 26, 2080–2087.

    Article  PubMed  CAS  Google Scholar 

  • Ciruela, F., Ferre, S., Casado, V., Cortes, A., Cunha, R.A., Lluis, C., and Franco, R. (2006b). Heterodimeric adenosine receptors: a device to regulate neurotransmitter release. Cell Mol. Life Sci. 63, 2427–2431.

    Article  PubMed  CAS  Google Scholar 

  • Corbit, L.H., Nie, H., and Janak, P.H. (2012). Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol. Psychiatry 72, 389–395.

    Article  PubMed  Google Scholar 

  • Diamond, I., Nagy, L., Mochly-Rosen, D., and Gordon, A. (1991). The role of adenosine and adenosine transport in ethanolinduced cellular tolerance and dependence. Possible biologic and genetic markers of alcoholism. Ann. NY Acad. Sci. 625, 473–487.

    Article  PubMed  CAS  Google Scholar 

  • Dore, A.S., Robertson, N., Errey, J.C., Ng, I., Hollenstein, K., Tehan, B., Hurrell, E., Bennett, K., Congreve, M., Magnani, F., et al. (2011). Structure of the adenosine A(2A) receptor in complex with ZM241385 and the xanthines XAC and caffeine. Structure 19, 1283–1293.

    Article  PubMed  CAS  Google Scholar 

  • Dunwiddie, T.V., and Masino, S.A. (2001). The role and regulation of adenosine in the central nervous system. Annu. Rev. Neurosci. 24, 31–55.

    Article  PubMed  CAS  Google Scholar 

  • Durieux, P.F., Schiffmann, S.N., and de Kerchove d’Exaerde, A. (2011). Targeting neuronal populations of the striatum. Front Neuroanat. 5, 40.

    Article  PubMed  CAS  Google Scholar 

  • El Yacoubi, M., Ledent, C., Menard, J.F., Parmentier, M., Costentin, J., and Vaugeois, J.M. (2000). The stimulant effects of caffeine on locomotor behaviour in mice are mediated through its blockade of adenosine A(2A) receptors. Br. J. Pharmacol. 129, 1465–1473.

    Article  PubMed  Google Scholar 

  • El Yacoubi, M., Ledent, C., Parmentier, M., Daoust, M., Costentin, J., and Vaugeois, J. (2001). Absence of the adenosine A(2A) receptor or its chronic blockade decrease ethanol withdrawalinduced seizures in mice. Neuropharmacology 40, 424–432.

    Article  PubMed  Google Scholar 

  • Ena, S., de Kerchove d’Exaerde, A., and Schiffmann, S.N. (2011). Unraveling the differential functions and regulation of striatal neuron sub-populations in motor control, reward, and motivational processes. Front. Behav. Neurosci. 5, 47.

    Article  PubMed  Google Scholar 

  • Everitt, B.J., and Robbins, T.W. (2013). From the ventral to the dorsal striatum: devolving views of their roles in drug addiction. Neurosci. Biobehav. Rev. [Epub ahead of print].

    Google Scholar 

  • Ferré, S., Fredholm, B.B., Morelli, M., Popoli, P., and Fuxe, K. (1997). Adenosine-dopamine receptor-receptor interactions as an integrative mechanism in the basal ganglia. Trends Neurosci. 20, 482–487.

    Article  PubMed  Google Scholar 

  • Fredholm, B.B., Chen, J.F., Cunha, R.A., Svenningsson, P., and Vaugeois, J.M. (2005a). Adenosine and brain function. Int. Rev. Neurobiol. 63, 191–270.

    Article  PubMed  CAS  Google Scholar 

  • Fredholm, B.B., Chen, J.F., Masino, S.A., and Vaugeois, J.M. (2005b). Actions of adenosine at its receptors in the CNS: insights from knockouts and drugs. Annu. Rev. Pharmacol. Toxicol. 45, 385–412.

    Article  PubMed  CAS  Google Scholar 

  • Froehlich, J.C., Zweifel, M., Harts, J., Lumeng, L., and Li, T.K. (1991). Importance of delta opioid receptors in maintaining high alcohol drinking. Psychopharmacology 103, 467–472.

    Article  PubMed  CAS  Google Scholar 

  • Fuxe, K., Ferre, S., Genedani, S., Franco, R., and Agnati, L.F. (2007). Adenosine receptor-dopamine receptor interactions in the basal ganglia and their relevance for brain function. Physiol. Behav. 92, 210–217.

    Article  PubMed  CAS  Google Scholar 

  • Fuxe, K., Marcellino, D., Borroto-Escuela, D.O., Guescini, M., Fernandez-Duenas, V., Tanganelli, S., Rivera, A., Ciruela, F., and Agnati, L.F. (2010). Adenosine-dopamine interactions in the pathophysiology and treatment of CNS disorders. CNS Neurosci. Ther. 16, e18–42.

    Article  PubMed  CAS  Google Scholar 

  • Gong, S., Zheng, C., Doughty, M.L., Losos, K., Didkovsky, N., Schambra, U.B., Nowak, N.J., Joyner, A., Leblanc, G., Hatten, M.E., et al. (2003). A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425, 917–925.

    Article  PubMed  CAS  Google Scholar 

  • Gordon, A.S., and Diamond, I. (1993). Adenosine mediates the effects of ethanol on the cAMP signal transduction system. Alcohol. Alcohol. Suppl. 2, 437–441.

    PubMed  CAS  Google Scholar 

  • Graybiel, A.M. (2000). The basal ganglia. Curr. Biol. 10, R509–511.

    Article  PubMed  CAS  Google Scholar 

  • Graybiel, A.M. (2008). Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 31, 359–387.

    Article  PubMed  CAS  Google Scholar 

  • Herz, A. (1997). Endogenous opioid systems and alcohol addiction. Psychopharmacology 129, 99–111.

    Article  PubMed  CAS  Google Scholar 

  • Huang, Z.L., Qu, W.M., Eguchi, N., Chen, J.F., Schwarzschild, M.A., Fredholm, B.B., Urade, Y., and Hayaishi, O. (2005). Adenosine A2A, but not A1, receptors mediate the arousal effect of caffeine. Nat. Neurosci. 8, 858–859.

    Article  PubMed  CAS  Google Scholar 

  • Humphries, M.D., and Prescott, T.J. (2010). The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy, and reward. Prog. Neurobiol. 90, 385–417.

    Article  PubMed  Google Scholar 

  • Jennings, L.L., Cass, C.E., Ritzel, M.W.L., Yao, S.Y.M., Young, J.D., Griffiths, M., and Baldwin, S.A. (1998). Adenosine transport: Recent advances in the molecular biology of nucleoside transporter proteins. Drug Dev. Res. 45, 277–287.

    Article  CAS  Google Scholar 

  • Jennings, L.L., Hao, C., Cabrita, M.A., Vickers, M.F., Baldwin, S.A., Young, J.D., and Cass, C.E. (2001). Distinct regional distribution of human equilibrative nucleoside transporter proteins 1 and 2 (hENT1 and hENT2) in the central nervous system. Neuropharmacology 40, 722–731.

    Article  PubMed  CAS  Google Scholar 

  • Kaplan, G.B., Bharmal, N.H., Leite-Morris, K.A., and Adams, W.R. (1999). Role of adenosine A1 and A2A receptors in the alcohol withdrawal syndrome. Alcohol 19, 157–162.

    Article  PubMed  CAS  Google Scholar 

  • Kim, J.H., Karpyak, V.M., Biernacka, J.M., Nam, H.W., Lee, M.R., Preuss, U.W., Zill, P., Yoon, G., Colby, C., Mrazek, D.A., et al. (2011). Functional role of the polymorphic 647 T/C variant of ENT1 (SLC29A1) and its association with alcohol withdrawal seizures. PLoS One 6, e16331.

    Article  PubMed  CAS  Google Scholar 

  • King, A.E., Ackley, M.A., Cass, C.E., Young, J.D., and Baldwin, S.A. (2006). Nucleoside transporters: from scavengers to novel therapeutic targets. Trends Pharmacol. Sci. 27, 416–425.

    Article  PubMed  CAS  Google Scholar 

  • Koob, G.F., and Volkow, N.D. (2010). Neurocircuitry of addiction. Neuropsychopharmacology 35, 217–238.

    Article  PubMed  Google Scholar 

  • Kulik, T.B., Aronhime, S.N., Echeverry, G., Beylin, A., and Winn, H.R. (2010). The relationship between oxygen and adenosine in astrocytic cultures. Glia 58, 1335–1344.

    PubMed  Google Scholar 

  • Kull, B., Svenningsson, P., and Fredholm, B.B. (2000). Adenosine A(2A) receptors are colocalized with and activate g(olf) in rat striatum. Mol. Pharmacol. 58, 771–777.

    PubMed  CAS  Google Scholar 

  • Le Moine, C., and Bloch, B. (1995). D1 and D2 dopamine receptor gene expression in the rat striatum: sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNAs in distinct neuronal populations of the dorsal and ventral striatum. J. Comp. Neurol. 355, 418–426.

    Article  PubMed  Google Scholar 

  • Ledent, C., Vaugeois, J.M., Schiffmann, S.N., Pedrazzini, T., El Yacoubi, M., Vanderhaeghen, J.J., Costentin, J., Heath, J.K., Vassart, G., and Parmentier, M. (1997). Aggressiveness, hypoalgesia and high blood pressure in mice lacking the adenosine A2a receptor. Nature 388, 674–678.

    Article  PubMed  CAS  Google Scholar 

  • Li, X.W., Li, T.K., and Froehlich, J.C. (1998). Enhanced sensitivity of the nucleus accumbens proenkephalin system to alcohol in rats selectively bred for alcohol preference. Brain Res. 794, 35–47.

    Article  PubMed  CAS  Google Scholar 

  • Lloyd, H.G., and Schrader, J. (1993). Adenosine metabolism in the guinea pig heart: the role of cytosolic S-adenosyl-L-homocysteine hydrolase, 5′-nucleotidase and adenosine kinase. Eur. Heart J. 14 Suppl I, 27–33.

    Google Scholar 

  • Lobo, M.K., Karsten, S.L., Gray, M., Geschwind, D.H., and Yang, X.W. (2006). FACS-array profiling of striatal projection neuron subtypes in juvenile and adult mouse brains. Nat. Neurosci. 9, 443–452.

    Article  PubMed  CAS  Google Scholar 

  • Lobo, M.K., Cui, Y., Ostlund, S.B., Balleine, B.W., and Yang, X.W. (2007). Genetic control of instrumental conditioning by striatopallidal neuron-specific S1P receptor Gpr6. Nat. Neurosci. 10, 1395–1397.

    Article  PubMed  CAS  Google Scholar 

  • Lonze, B.E., and Ginty, D.D. (2002). Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605–623.

    Article  PubMed  CAS  Google Scholar 

  • Lovinger, D.M. (2010). Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 58, 951–961.

    Article  PubMed  CAS  Google Scholar 

  • Mendez, M., and Morales-Mulia, M. (2006). Ethanol exposure differentially alters pro-enkephalin mRNA expression in regions of the mesocorticolimbic system. Psychopharmacology 189, 117–124.

    Article  PubMed  CAS  Google Scholar 

  • Meng, Z.H., and Dar, M.S. (1995). Possible role of striatal adenosine in the modulation of acute ethanol-induced motor incoordination in rats. Alcohol. Clin. Exp. Res. 19, 892–901.

    Article  PubMed  CAS  Google Scholar 

  • Naassila, M., Ledent, C., and Daoust, M. (2002). Low ethanol sensitivity and increased ethanol consumption in mice lacking adenosine A2A receptors. J. Neurosci. 22, 10487–10493.

    PubMed  CAS  Google Scholar 

  • Nagy, L.E., and DeSilva, S.E. (1994). Adenosine A1 receptors mediate chronic ethanol-induced increases in receptor-stimulated cyclic AMP in cultured hepatocytes. Biochem. J. 304(Pt 1), 205–210.

    PubMed  CAS  Google Scholar 

  • Nam, H.W., Lee, M.R., Zhu, Y., Wu, J., Hinton, D.J., Choi, S., Kim, T., Hammack, N., Yin, J.C., and Choi, D.S. (2011). Type 1 equilibrative nucleoside transporter regulates ethanol drinking through accumbal N-methyl-D-aspartate receptor signaling. Biol. Psychiatry 69, 1043–1051.

    Article  PubMed  CAS  Google Scholar 

  • Nam, H.W., McIver, S.R., Hinton, D.J., Thakkar, M.M., Sari, Y., Parkinson, F.E., Haydon, P.G., and Choi, D.-S. (2012). Adenosine and glutamate signaling in neuron-glial interactions: Implication in alcoholism and sleep disorders. Alcohol. Clin. Exp. Ther. 36, 1117–1125.

    Article  CAS  Google Scholar 

  • Nam, H.W., Hinton, D.J., Kang, N.Y., Kim, T., Lee, M.R., Oliveros, A., Adams, C., Ruby, C.L., and Choi, D.S. (2013). Adenosine transporter ENT1 regulates the acquisition of goal-directed behavior and ethanol drinking through A2A receptor in the dorsomedial striatum. J. Neurosci. 33, 4329–4338.

    Article  PubMed  CAS  Google Scholar 

  • Ng, G.Y., O’Dowd, B.F., and George, S.R. (1996). Genotypic differences in mesolimbic enkephalin gene expression in DBA/2J and C57BL/6J inbred mice. Eur. J. Pharmacol. 311, 45–52.

    Article  PubMed  CAS  Google Scholar 

  • Parkinson, F.E., Ferguson, J., Zamzow, C.R., and Xiong, W. (2006). Gene expression for enzymes and transporters involved in regulating adenosine and inosine levels in rat forebrain neurons, astrocytes and C6 glioma cells. J. Neurosci. Res. 84, 801–808.

    Article  PubMed  CAS  Google Scholar 

  • Pedata, F., Pazzagli, M., Tilli, S., and Pepeu, G. (1990). Regional differences in the electrically stimulated release of endogenous and radioactive adenosine and purine derivatives from rat brain slices. Naunyn Schmiedebergs Arch. Pharmacol. 342, 447–453.

    Article  PubMed  CAS  Google Scholar 

  • Ruby, C.L., Adams, C., Knight, E.J., Nam, H.W., and Choi, D.S. (2010). An essential role for adenosine signaling in alcohol abuse. Curr. Drug Abuse Rev. 3, 163–174.

    Article  PubMed  CAS  Google Scholar 

  • Surmeier, D.J., Song, W.J., and Yan, Z. (1996). Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J. Neurosci. 16, 6579–6591.

    PubMed  CAS  Google Scholar 

  • Surmeier, D.J., Ding, J., Day, M., Wang, Z., and Shen, W. (2007). D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci. 30, 228–235.

    Article  PubMed  CAS  Google Scholar 

  • Svenningsson, P., Le Moine, C., Fisone, G., and Fredholm, B.B. (1999). Distribution, biochemistry and function of striatal adenosine A2A receptors. Prog. Neurobiol. 59, 355–396.

    Article  PubMed  CAS  Google Scholar 

  • Voorn, P., Vanderschuren, L.J., Groenewegen, H.J., Robbins, T.W., and Pennartz, C.M. (2004). Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci. 27, 468–474.

    Article  PubMed  CAS  Google Scholar 

  • Yang, X., Horn, K., and Wand, G.S. (1998). Chronic ethanol exposure impairs phosphorylation of CREB and CRE-binding activity in rat striatum. Alcohol. Clin. Exp. Res. 22, 382–390.

    Article  PubMed  CAS  Google Scholar 

  • Yao, S.Y., Ng, A.M., Muzyka, W.R., Griffiths, M., Cass, C.E., Baldwin, S.A., and Young, J.D. (1997). Molecular cloning and functional characterization of nitrobenzylthioinosine (NBMPR)-sensitive (es) and NBMPR-insensitive (ei) equilibrative nucleoside transporter proteins (rENT1 and rENT2) from rat tissues. J. Biol. Chem. 272, 28423–28430.

    Article  PubMed  CAS  Google Scholar 

  • Yao, L., McFarland, K., Fan, P., Jiang, Z., Ueda, T., and Diamond, I. (2006). Adenosine A2a blockade prevents synergy between muopiate and cannabinoid CB1 receptors and eliminates heroin-seeking behavior in addicted rats. Proc. Natl. Acad. Sci. USA 103, 7877–7882.

    Article  PubMed  CAS  Google Scholar 

  • Yin, H.H., and Knowlton, B.J. (2006). The role of the basal ganglia in habit formation. Nat. Rev. Neurosci. 7, 464–476.

    Article  PubMed  CAS  Google Scholar 

  • Yin, H.H., Knowlton, B.J., and Balleine, B.W. (2004). Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J. Neurosci. 19, 181–189.

    Article  PubMed  Google Scholar 

  • Yin, H.H., Park, B.S., Adermark, L., and Lovinger, D.M. (2007). Ethanol reverses the direction of long-term synaptic plasticity in the dorsomedial striatum. Eur. J. Neurosci. 25, 3226–3232.

    Article  PubMed  Google Scholar 

  • Yin, H.H., Mulcare, S.P., Hilario, M.R., Clouse, E., Holloway, T., Davis, M.I., Hansson, A.C., Lovinger, D.M., and Costa, R.M. (2009). Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat. Neurosci. 12, 333–341.

    Article  PubMed  CAS  Google Scholar 

  • Yu, C., Gupta, J., Chen, J.F., and Yin, H.H. (2009). Genetic deletion of A2A adenosine receptors in the striatum selectively impairs habit formation. J. Neurosci. 29, 15100–15103.

    Article  PubMed  CAS  Google Scholar 

  • Zahniser, N.R., Simosky, J.K., Mayfield, R.D., Negri, C.A., Hanania, T., Larson, G.A., Kelly, M.A., Grandy, D.K., Rubinstein, M., Low, M.J., et al. (2000). Functional uncoupling of adenosine A(2A) receptors and reduced responseto caffeine in mice lacking dopamine D2 receptors. J. Neurosci. 20, 5949–5957.

    PubMed  CAS  Google Scholar 

  • Zamzow, C.R., Xiong, W., and Parkinson, F.E. (2008). Astrocytes affect the profile of purines released from cultured cortical neurons. J. Neurosci. Res. 86, 2641–2649.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Pharmacology and Experimental Therapeutics, Mayo Clinic College of Medicine, Rochester, Minnesota, 55905, USA

    Hyung Wook Nam & Doo-Sup Choi

  2. Department of Psychiatry and Psychology, Mayo Clinic College of Medicine, Rochester, Minnesota, 55905, USA

    Hyung Wook Nam & Doo-Sup Choi

  3. Molecular Neuroscience Program, Mayo Clinic College of Medicine, Rochester, Minnesota, 55905, USA

    Robert C. Bruner & Doo-Sup Choi

Authors
  1. Hyung Wook Nam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert C. Bruner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Doo-Sup Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Doo-Sup Choi.

About this article

Cite this article

Nam, H.W., Bruner, R.C. & Choi, DS. Adenosine signaling in striatal circuits and alcohol use disorders. Mol Cells 36, 195–202 (2013). https://doi.org/10.1007/s10059-013-0192-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10059-013-0192-9

Keywords

Search

Navigation