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Role of dopamine D2-like receptors and their modulation by adenosine receptor stimulation in the reinstatement of methamphetamine seeking

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Abstract

Rationale and objective

Previous work has demonstrated that dopamine and adenosine receptors are involved in drug-seeking behaviors, yet the pharmacological interactions between these receptors in methamphetamine (MA) seeking are not well characterized. The present studies examined the role of the dopamine D2-like receptors in MA seeking and identified the interactive effects of adenosine receptor stimulation.

Methods

Adult male Sprague–Dawley rats were trained to lever press for MA in daily 2-h self-administration sessions on a fixed-ratio 1 schedule for 10 consecutive days. After 1 day of abstinence, lever pressing was extinguished in six daily extinction sessions. Treatments were administered systemically prior to a 2-h reinstatement test session.

Results

An increase in MA seeking was observed following the administration of the dopamine D2-like agonist, quinpirole, or the D3 receptor agonist, 7-OH-DPAT. Stimulation of D2 or D4 receptors was ineffective at inducing MA seeking. Quinpirole-induced MA seeking was inhibited by D3 receptor antagonism (SB-77011A or PG01037), an adenosine A1 agonist, CPA, and an adenosine A2A agonist, CGS 21680. MA seeking induced by a MA priming injection or D3 receptor stimulation was inhibited by a pretreatment with the adenosine A1 agonist, CPA, but not the adenosine A2A agonist, CGS 21680.

Conclusions

These results demonstrate the sufficiency of dopamine D3 receptors to reinstate MA seeking that is inhibited when combined with adenosine A1 receptor stimulation.

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References

  • Ahlenius S, Salmi P (1994) Behavioral and biochemical effects of the dopamine D3 receptor-selective ligand, 7-OH-DPAT, in the normal and the reserpine-treated rat. Eur J Pharmacol 260:177–181

    Article  CAS  PubMed  Google Scholar 

  • Ariano MA, Wang J, Noblett KL, Larson ER, Sibley DR (1997) Cellular distribution of the rat D4 dopamine receptor protein in the CNS using anti-receptor antisera. Brain Res 752:26–34

    Article  CAS  PubMed  Google Scholar 

  • Bachtell RK, Self DW (2009) Effects of adenosine a(2A) receptor stimulation on cocaine-seeking behavior in rats. Psychopharmacol Berl 206:469–478. https://doi.org/10.1007/s00213-009-1624-2

    Article  CAS  Google Scholar 

  • Bachtell RK, Whisler K, Karanian D, Self DW (2005) Effects of intra-nucleus accumbens shell administration of dopamine agonists and antagonists on cocaine-taking and cocaine-seeking behaviors in the rat. Psychopharmacol Berl 183:41–53

    Article  CAS  Google Scholar 

  • Bardo MT, Valone JM, Bevins RA (1999) Locomotion and conditioned place preference produced by acute intravenous amphetamine: role of dopamine receptors and individual differences in amphetamine self-administration. Psychopharmacol Berl 143:39–46

    Article  CAS  Google Scholar 

  • Barrie AP, Nicholls DG (1993) Adenosine A1 receptor inhibition of glutamate exocytosis and protein kinase C-mediated decoupling. J Neurochem 60:1081–1086

    Article  CAS  PubMed  Google Scholar 

  • Borroto-Escuela DO, Wydra K, Li X, Rodriguez D, Carlsson J, Jastrzębska J, Filip M, Fuxe K (2018) Disruption of A2AR-D2R Heteroreceptor complexes after A2AR transmembrane 5 peptide administration enhances cocaine self-administration in rats. Mol Neurobiol 55:7038–7048. https://doi.org/10.1007/s12035-018-0887-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brennan KA, Carati C, Lea RA, Fitzmaurice PS, Schenk S (2009) Effect of D1-like and D2-like receptor antagonists on methamphetamine and 3,4-methylenedioxymethamphetamine self-administration in rats. Behav Pharmacol 20:688–694. https://doi.org/10.1097/FBP.0b013e328333a28d

    Article  CAS  PubMed  Google Scholar 

  • Brown JM, Hanson GR, Fleckenstein AE (2000) Methamphetamine rapidly decreases vesicular dopamine uptake. J Neurochem 74:2221–2223

    Article  CAS  PubMed  Google Scholar 

  • Burris KD, Pacheco MA, Filtz TM, Kung MP, Kung HF, Molinoff PB (1995) Lack of discrimination by agonists for D2 and D3 dopamine receptors. Neuropsychopharmacology 12:335–345. https://doi.org/10.1016/0893-133X(94)00099-L

    Article  CAS  PubMed  Google Scholar 

  • Carati C, Schenk S (2011) Role of dopamine D1- and D2-like receptor mechanisms in drug-seeking following methamphetamine self-administration in rats. Pharmacol Biochem Behav 98:449–454. https://doi.org/10.1016/j.pbb.2011.02.010

    Article  CAS  PubMed  Google Scholar 

  • Cass CE, Belt JA, Paterson AR (1987) Adenosine transport in cultured cells and erythrocytes. Prog Clin Biol Res 230:13–40

    CAS  PubMed  Google Scholar 

  • Chen Y, Song R, Yang R-F, Wu N, Li J (2014) A novel dopamine D3 receptor antagonist YQA14 inhibits methamphetamine self-administration and relapse to drug-seeking behaviour in rats. Eur J Pharmacol 743:126–132. https://doi.org/10.1016/j.ejphar.2014.09.026

    Article  CAS  PubMed  Google Scholar 

  • Chesworth R, Brown RM, Kim JH, Ledent C, Lawrence AJ (2016) Adenosine 2A receptors modulate reward behaviours for methamphetamine. Addict Biol 21:407–421. https://doi.org/10.1111/adb.12225

    Article  CAS  PubMed  Google Scholar 

  • Ciruela F, Casado V, Rodrigues RJ et al (2006) Presynaptic control of striatal glutamatergic neurotransmission by adenosine A1–A2A receptor heteromers. J Neurosci 26:2080–2087. https://doi.org/10.1523/JNEUROSCI.3574-05.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Copeland AL, Sorensen JL (2001) Differences between methamphetamine users and cocaine users in treatment. Drug Alcohol Depend 62:91–95

    Article  CAS  PubMed  Google Scholar 

  • Cox BM, Young AB, See RE, Reichel CM (2013) Sex differences in methamphetamine seeking in rats: impact of oxytocin. Psychoneuroendocrinology 38:2343–2353. https://doi.org/10.1016/j.psyneuen.2013.05.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daly SA, Waddington JL (1993) Behavioural effects of the putative D-3 dopamine receptor agonist 7-OH-DPAT in relation to other “D-2-like” agonists. Neuropharmacology 32:509–510

    Article  CAS  PubMed  Google Scholar 

  • De Boer P, Enrico P, Wright J et al (1997) Characterization of the effect of dopamine D3 receptor stimulation on locomotion and striatal dopamine levels. Brain Res 758:83–91

    Article  PubMed  Google Scholar 

  • De Vries TJ, Schoffelmeer AN, Binnekade R et al (2002) Relapse to cocaine- and heroin-seeking behavior mediated by dopamine D2 receptors is time-dependent and associated with behavioral sensitization. Neuropsychopharmacology 26:18–26

    Article  PubMed  Google Scholar 

  • Depoortere R, Perrault G, Sanger DJ (1996) Behavioural effects in the rat of the putative dopamine D3 receptor agonist 7-OH-DPAT: comparison with quinpirole and apomorphine. Psychopharmacology 124:231–240

    Article  CAS  PubMed  Google Scholar 

  • Duarte C, Biala G, Le Bihan C et al (2003) Respective roles of dopamine D2 and D3 receptors in food-seeking behaviour in rats. Psychopharmacology 166:19–32. https://doi.org/10.1007/s00213-002-1310-0

    Article  CAS  PubMed  Google Scholar 

  • Ferrari F, Giuliani D (1995) Behavioural effects of the dopamine D3 receptor agonist 7-OH-DPAT in rats. Pharmacol Res 32:63–68

    Article  CAS  PubMed  Google Scholar 

  • Filip M, Frankowska M, Zaniewska M, Przegaliński E, Műller CE, Agnati L, Franco R, Roberts DCS, Fuxe K (2006) Involvement of adenosine A2A and dopamine receptors in the locomotor and sensitizing effects of cocaine. Brain Res 1077:67–80

    Article  CAS  PubMed  Google Scholar 

  • Filip M, Zaniewska M, Frankowska M, Wydra K, Fuxe K (2012) The importance of the adenosine a(2A) receptor–dopamine D(2) receptor interaction in drug addiction. Curr Med Chem 19:317–355

    Article  CAS  PubMed  Google Scholar 

  • Fleckenstein AE, Metzger RR, Gibb JW, Hanson GR (1997) A rapid and reversible change in dopamine transporters induced by methamphetamine. Eur J Pharmacol 323:R9–R10

    Article  CAS  PubMed  Google Scholar 

  • Fredholm BB, Fried G, Hedqvist P (1982) Origin of adenosine released from rat vas deferens by nerve stimulation. Eur J Pharmacol 79:233–243

    Article  CAS  PubMed  Google Scholar 

  • Fuchs RA, Tran-Nguyen LTL, Weber SM, Khroyan TV, Neisewander JL (2002) Effects of 7-OH-DPAT on cocaine-seeking behavior and on re-establishment of cocaine self-administration. Pharmacol Biochem Behav 72:623–632

    Article  CAS  PubMed  Google Scholar 

  • Golembiowska K, Zylewska A (1998) N6-2-(4-aminophenyl)ethyladenosine (APNEA), a putative adenosine A3 receptor agonist, enhances methamphetamine-induced dopamine outflow in rat striatum. Pol J Pharmacol 50:299–305

    CAS  PubMed  Google Scholar 

  • Graham DL, Hoppenot R, Hendryx A, Self DW (2007) Differential ability of D1 and D2 dopamine receptor agonists to induce and modulate expression and reinstatement of cocaine place preference in rats. Psychopharmacol Berl 191:719–730. https://doi.org/10.1007/s00213-006-0473-5

    Article  CAS  Google Scholar 

  • Griffon N, Pilon C, Sautel F, Schwartz JC, Sokoloff P (1996) (1996) antipsychotics with inverse agonist activity at the dopamine D3 receptor. J Neural Transm Vienna Austria 103:1163–1175. https://doi.org/10.1007/BF01271201

    Article  CAS  Google Scholar 

  • Grundt P, Prevatt KM, Cao J, Taylor M, Floresca CZ, Choi JK, Jenkins BG, Luedtke RR, Newman AH (2007) Heterocyclic analogues of N-(4-(4-(2,3-dichlorophenyl)piperazin-1-yl)butyl) arylcarboxamides with functionalized linking chains as novel dopamine D3 receptor ligands: potential substance abuse therapeutic agents. J Med Chem 50:4135–4146. https://doi.org/10.1021/jm0704200

    Article  CAS  PubMed  Google Scholar 

  • Gurevich EV, Joyce JN (1999) Distribution of dopamine D3 receptor expressing neurons in the human forebrain: comparison with D2 receptor expressing neurons. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 20:60–80. https://doi.org/10.1016/S0893-133X(98)00066-9

    Article  CAS  Google Scholar 

  • Hall H, Köhler C, Gawell L (1985) Some in vitro receptor binding properties of [3H] eticlopride, a novel substituted benzamide, selective for dopamine-D2 receptors in the rat brain. Eur J Pharmacol 111:191–199

    Article  CAS  PubMed  Google Scholar 

  • Hartz DT, Frederick-Osborne SL, Galloway GP (2001) Craving predicts use during treatment for methamphetamine dependence: a prospective, repeated-measures, within-subject analysis. Drug Alcohol Depend 63:269–276

    Article  CAS  PubMed  Google Scholar 

  • Higley AE, Kiefer SW, Li X, Gaál J, Xi ZX, Gardner EL (2011a) Dopamine D(3) receptor antagonist SB-277011A inhibits methamphetamine self-administration and methamphetamine-induced reinstatement of drug-seeking in rats. Eur J Pharmacol 659:187–192. https://doi.org/10.1016/j.ejphar.2011.02.046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higley AE, Spiller K, Grundt P et al (2011b) PG01037, a novel dopamine D3 receptor antagonist, inhibits the effects of methamphetamine in rats. J Psychopharmacol Oxf Engl 25:263–273. https://doi.org/10.1177/0269881109358201

    Article  CAS  Google Scholar 

  • Hobson BD, Merritt KE, Bachtell RK (2012) Stimulation of adenosine receptors in the nucleus accumbens reverses the expression of cocaine sensitization and cross-sensitization to dopamine D2 receptors in rats. Neuropharmacology 63:1172–1181. https://doi.org/10.1016/j.neuropharm.2012.06.038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hobson BD, O’Neill CE, Levis SC et al (2013) Adenosine A1 and dopamine d1 receptor regulation of AMPA receptor phosphorylation and cocaine-seeking behavior. Neuropsychopharmacology 38:1974–1983. https://doi.org/10.1038/npp.2013.96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kavanagh KA, Schreiner DC, Levis SC, O'Neill CE, Bachtell RK (2015) Role of adenosine receptor subtypes in methamphetamine reward and reinforcement. Neuropharmacology 89:265–273. https://doi.org/10.1016/j.neuropharm.2014.09.030

    Article  CAS  PubMed  Google Scholar 

  • Khroyan TV, Baker DA, Neisewander JL (1995) Dose-dependent effects of the D3-preferring agonist 7-OH-DPAT on motor behaviors and place conditioning. Psychopharmacology 122:351–357

    Article  CAS  PubMed  Google Scholar 

  • Khroyan TV, Barrett-Larimore RL, Rowlett JK, Spealman RD (2000) Dopamine D1- and D2-like receptor mechanisms in relapse to cocaine-seeking behavior: effects of selective antagonists and agonists. J Pharmacol Exp Ther 294:680–687

    CAS  PubMed  Google Scholar 

  • Kitamura O, Wee S, Specio SE, Koob GF, Pulvirenti L (2006) Escalation of methamphetamine self-administration in rats: a dose–effect function. Psychopharmacology 186:48–53. https://doi.org/10.1007/s00213-006-0353-z

    Article  CAS  PubMed  Google Scholar 

  • Levant B, Bancroft GN, Selkirk CM (1996) In vivo occupancy of D2 dopamine receptors by 7-OH-DPAT. Synapse 24:60–64

    Article  CAS  PubMed  Google Scholar 

  • Levesque D, Diaz J, Pilon C, Martres MP, Giros B, Souil E, Schott D, Morgat JL, Schwartz JC, Sokoloff P (1992) Identification, characterization, and localization of the dopamine D3 receptor in rat brain using 7-[3H]hydroxy-N,N-di-n-propyl-2-aminotetralin. Proc Natl Acad Sci U S A 89:8155–8159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchi M, Raiteri L, Risso F, Vallarino A, Bonfanti A, Monopoli A, Ongini E, Raiteri M (2002) Effects of adenosine A1 and A2A receptor activation on the evoked release of glutamate from rat cerebrocortical synaptosomes. Br J Pharmacol 136:434–440. https://doi.org/10.1038/sj.bjp.0704712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto JPP, Almeida MG, Castilho-Martins EA, Costa MA, Fior-Chadi DR (2014) Protein kinase A mediates adenosine A2a receptor modulation of neurotransmitter release via synapsin I phosphorylation in cultured cells from medulla oblongata. Neurosci Res 85:1–11. https://doi.org/10.1016/j.neures.2014.05.007

    Article  CAS  PubMed  Google Scholar 

  • McCall RB, Lookingland KJ, Bédard PJ, Huff RM (2005) Sumanirole, a highly dopamine D2-selective receptor agonist: in vitro and in vivo pharmacological characterization and efficacy in animal models of Parkinson’s disease. J Pharmacol Exp Ther 314:1248–1256. https://doi.org/10.1124/jpet.105.084202

    Article  CAS  PubMed  Google Scholar 

  • Meyer ME (1996) Mesolimbic 7-OH-DPAT affects locomotor activities in rats. Pharmacol Biochem Behav 55:209–214

    Article  CAS  PubMed  Google Scholar 

  • Milesi-Hallé A, McMillan DE, Laurenzana EM et al (2007) Sex differences in (+)-amphetamine- and (+)-methamphetamine-induced behavioral response in male and female Sprague-Dawley rats. Pharmacol Biochem Behav 86:140–149. https://doi.org/10.1016/j.pbb.2006.12.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreland RB, Patel M, Hsieh GC, Wetter JM, Marsh K, Brioni JD (2005) A-412997 is a selective dopamine D4 receptor agonist in rats. Pharmacol Biochem Behav 82:140–147. https://doi.org/10.1016/j.pbb.2005.08.001

    Article  CAS  PubMed  Google Scholar 

  • Munzar P, Goldberg SR (2000) Dopaminergic involvement in the discriminative-stimulus effects of methamphetamine in rats. Psychopharmacology 148:209–216

    Article  CAS  PubMed  Google Scholar 

  • NIDA (2013) Epidemiologic trends in drug abuse

  • O’Neill CE, LeTendre ML, Bachtell RK (2012) Adenosine A2A receptors in the nucleus accumbens bi-directionally alter cocaine seeking in rats. Neuropsychopharmacology 37:1245–1256. https://doi.org/10.1038/npp.2011.312

    Article  CAS  PubMed  Google Scholar 

  • Popoli P, Betto P, Reggio R, Ricciarello G (1995) Adenosine A2A receptor stimulation enhances striatal extracellular glutamate levels in rats. Eur J Pharmacol 287:215–217

    Article  CAS  PubMed  Google Scholar 

  • Quarta D, Ferre S, Solinas M et al (2004) Opposite modulatory roles for adenosine A1 and A2A receptors on glutamate and dopamine release in the shell of the nucleus accumbens. Effects of chronic caffeine exposure. J Neurochem 88:1151–1158

    Article  CAS  PubMed  Google Scholar 

  • Quiroz C, Lujan R, Uchigashima M et al (2009) Key modulatory role of presynaptic adenosine A2A receptors in cortical neurotransmission to the striatal direct pathway. ScientificWorldJournal 9:1321–1344. https://doi.org/10.1100/tsw.2009.143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reavill C, Taylor SG, Wood MD, Ashmeade T, Austin NE, Avenell KY, Boyfield I, Branch CL, Cilia J, Coldwell MC, Hadley MS, Hunter AJ, Jeffrey P, Jewitt F, Johnson CN, Jones DN, Medhurst AD, Middlemiss DN, Nash DJ, Riley GJ, Routledge C, Stemp G, Thewlis KM, Trail B, Vong AK, Hagan JJ (2000) Pharmacological actions of a novel, high-affinity, and selective human dopamine D(3) receptor antagonist, SB-277011-a. J Pharmacol Exp Ther 294:1154–1165

    CAS  PubMed  Google Scholar 

  • Reichel CM, Chan CH, Ghee SM, See RE (2012) Sex differences in escalation of methamphetamine self-administration: cognitive and motivational consequences in rats. Psychopharmacology 223:371–380. https://doi.org/10.1007/s00213-012-2727-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigues RJ, Alfaro TM, Rebola N, Oliveira CR, Cunha RA (2005) Co-localization and functional interaction between adenosine a(2A) and metabotropic group 5 receptors in glutamatergic nerve terminals of the rat striatum. J Neurochem 92:433–441. https://doi.org/10.1111/j.1471-4159.2004.02887.x

    Article  CAS  PubMed  Google Scholar 

  • Roth ME, Carroll ME (2004) Sex differences in the acquisition of IV methamphetamine self-administration and subsequent maintenance under a progressive ratio schedule in rats. Psychopharmacology 172:443–449. https://doi.org/10.1007/s00213-003-1670-0

    Article  CAS  PubMed  Google Scholar 

  • Ruda-Kucerova J, Amchova P, Babinska Z, Dusek L, Micale V, Sulcova A (2015) Sex differences in the reinstatement of methamphetamine seeking after forced abstinence in Sprague-Dawley rats. Front Psychiatry 6. https://doi.org/10.3389/fpsyt.2015.00091

  • Schiffmann SN, Jacobs O, Vanderhaeghen JJ (1991) Striatal restricted adenosine A2 receptor (RDC8) is expressed by enkephalin but not by substance P neurons: an in situ hybridization histochemistry study. J Neurochem 57:1062–1067

    Article  CAS  PubMed  Google Scholar 

  • Schindler CW, Bross JG, Thorndike EB (2002) Gender differences in the behavioral effects of methamphetamine. Eur J Pharmacol 442:231–235

    Article  CAS  PubMed  Google Scholar 

  • Schmidt HD, Anderson SM, Pierce RC (2006) Stimulation of D1-like or D2 dopamine receptors in the shell, but not the core, of the nucleus accumbens reinstates cocaine-seeking behaviour in the rat. Eur J Neurosci 23:219–228

    Article  PubMed  Google Scholar 

  • Seeman P, Van Tol HH (1994) Dopamine receptor pharmacology. Trends Pharmacol Sci 15:264–270

    Article  CAS  PubMed  Google Scholar 

  • Self DW (2004) Regulation of drug-taking and -seeking behaviors by neuroadaptations in the mesolimbic dopamine system. Neuropharmacology 47(Suppl 1):242–255. https://doi.org/10.1016/j.neuropharm.2004.07.005

    Article  CAS  PubMed  Google Scholar 

  • Self DW, Barnhart WJ, Lehman DA, Nestler EJ (1996) Opposite modulation of cocaine-seeking behavior by D1- and D2-like dopamine receptor agonists. Science 271:1586–1589

    Article  CAS  PubMed  Google Scholar 

  • Shen HY, Canas PM, Garcia-Sanz P, Lan JQ, Boison D, Moratalla R, Cunha RA, Chen JF (2013) Adenosine A(2)A receptors in striatal glutamatergic terminals and GABAergic neurons oppositely modulate psychostimulant action and DARPP-32 phosphorylation. PLoS One 8:e80902. https://doi.org/10.1371/journal.pone.0080902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sibley DR, Monsma FJ Jr, Shen Y (1993) Molecular neurobiology of dopaminergic receptors. Int Rev Neurobiol 35:391–415

    Article  CAS  PubMed  Google Scholar 

  • Sokoloff P, Giros B, Martres MP, Bouthenet ML, Schwartz JC (1990) Molecular cloning and characterization of a novel dopamine receptor (D3) as a target for neuroleptics. Nature 347:146–151. https://doi.org/10.1038/347146a0

    Article  CAS  PubMed  Google Scholar 

  • Sun L, Song R, Chen Y, Yang RF, Wu N, Su RB, Li J (2016) A selective D3 receptor antagonist YQA14 attenuates methamphetamine-induced behavioral sensitization and conditioned place preference in mice. Acta Pharmacol Sin 37:157–165. https://doi.org/10.1038/aps.2015.96

    Article  CAS  PubMed  Google Scholar 

  • Svenningsson P, Fourreau L, Bloch B, Fredholm BB, Gonon F, le Moine C (1999) Opposite tonic modulation of dopamine and adenosine on c-fos gene expression in striatopallidal neurons. Neuroscience 89:827–837 S0306-4522(98)00403-5 [pii]

    Article  CAS  PubMed  Google Scholar 

  • Svensson K, Carlsson A, Waters N (1994) Locomotor inhibition by the D3 ligand R-(+)-7-OH-DPAT is independent of changes in dopamine release. J Neural Transm Gen Sect 95:71–74

    Article  CAS  PubMed  Google Scholar 

  • Ujike H, Onoue T, Akiyama K, Hamamura T, Otsuki S (1989) Effects of selective D-1 and D-2 dopamine antagonists on development of methamphetamine-induced behavioral sensitization. Psychopharmacology 98:89–92

    Article  CAS  PubMed  Google Scholar 

  • Venniro M, Zhang M, Shaham Y, Caprioli D (2017) Incubation of methamphetamine but not heroin craving after voluntary abstinence in male and female rats. Neuropsychopharmacology 42:1126–1135. https://doi.org/10.1038/npp.2016.287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volz TJ, Hanson GR, Fleckenstein AE (2007) The role of the plasmalemmal dopamine and vesicular monoamine transporters in methamphetamine-induced dopaminergic deficits. J Neurochem 101:883–888. https://doi.org/10.1111/j.1471-4159.2006.04419.x

    Article  CAS  PubMed  Google Scholar 

  • White TD (1977) Direct detection of depolarisation-induced release of ATP from a synaptosomal preparation. Nature 267:67–68

    Article  CAS  PubMed  Google Scholar 

  • Wydra K, Golembiowska K, Zaniewska M, Kamińska K, Ferraro L, Fuxe K, Filip M (2013) Accumbal and pallidal dopamine, glutamate and GABA overflow during cocaine self-administration and its extinction in rats. Addict Biol 18:307–324. https://doi.org/10.1111/adb.12031

    Article  CAS  PubMed  Google Scholar 

  • Wydra K, Suder A, Borroto-Escuela DO, Filip M, Fuxe K (2015) On the role of a(2) a and D(2) receptors in control of cocaine and food-seeking behaviors in rats. Psychopharmacol Berl 232:1767–1778. https://doi.org/10.1007/s00213-014-3818-5

    Article  CAS  Google Scholar 

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Acknowledgments

This work was funded by National Institutes of Health (grant no. DA033358).

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  1. Tracey A. Larson and Madeline C. Winkler contributed equally to this work.

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  1. Department of Psychology and Neuroscience and Center for Neuroscience, University of Colorado Boulder, 2860 Wilderness Place, Boulder, CO, 80301, USA

    Tracey A. Larson, Madeline C. Winkler, Jacob Stafford, Sophia C. Levis, Casey E. O’Neill & Ryan K. Bachtell

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Larson, T.A., Winkler, M.C., Stafford, J. et al. Role of dopamine D2-like receptors and their modulation by adenosine receptor stimulation in the reinstatement of methamphetamine seeking. Psychopharmacology 236, 1207–1218 (2019). https://doi.org/10.1007/s00213-018-5126-y

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