Adenosine receptor-mediated modulation of dopamine release in the nucleus accumbens depends on glutamate neurotransmission and N-methyl-D-aspartate receptor stimulation

Davide Quarta, Janusz Borycz, Marcello Solinas, Kshitij Patkar, Jörg Hockemeyer, Francisco Ciruela, Carme Lluis, Rafael Franco, Amina S. Woods, Steven R. Goldberg, Sergi Ferré

Research output: Contribution to journalArticle

Abstract

Adenosine, by acting on adenosine A1 and A2A receptors, exerts opposite modulatory roles on striatal extracellular levels of glutamate and dopamine, with activation of A1 inhibiting and activation of A2A receptors stimulating glutamate and dopamine release. Adenosine-mediated modulation of striatal dopaminergic neurotransmission could be secondary to changes in glutamate neurotransmission, in view of evidence for a preferential colocalization of A1 and A2A receptors in glutamatergic nerve terminals. By using in vivo microdialysis techniques, local perfusion of NMDA (3, 10 μM), the selective A2A receptor agonist 2-p-(2-carboxyethyl)phenethylamino-5′-N- ethylcarboxamidoadenosine (CGS 21680; 3, 10 μM), the selective A1 receptor antagonist 8-cyclopentyl-1,3-dimethylxanthine (CPT; 300, 1000 μM), or the non-selective A1-A2A receptor antagonist in vitro caffeine (300, 1000 μM) elicited significant increases in extracellular levels of dopamine in the shell of the nucleus accumbens (NAc). Significant glutamate release was also observed with local perfusion of CGS 21680, CPT and caffeine, but not NMDA. Co-perfusion with the competitive NMDA receptor antagonist DL-2-amino-5-phosphonovaleric acid (APV; 100 μM) counteracted dopamine release induced by NMDA, CGS 21680, CPT and caffeine. Co-perfusion with the selective A2A receptor antagonist MSX-3 (1 μM) counteracted dopamine and glutamate release induced by CGS 21680, CPT and caffeine and did not modify dopamine release induced by NMDA. These results indicate that modulation of dopamine release in the shell of the NAc by A1 and A2A receptors is mostly secondary to their opposite modulatory role on glutamatergic neurotransmission and depends on stimulation of NMDA receptors. Furthermore, these results underscore the role of A1 vs. A 2A receptor antagonism in the central effects of caffeine.

Original languageEnglish (US)
Pages (from-to)873-880
Number of pages8
JournalJournal of Neurochemistry
Volume91
Issue number4
DOIs
StatePublished - Nov 2004
Externally publishedYes

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Purinergic P1 Receptors
Nucleus Accumbens
N-Methyl-D-Aspartate Receptors
Synaptic Transmission
Glutamic Acid
Caffeine
Dopamine
Modulation
N-Methylaspartate
Perfusion
Corpus Striatum
Adenosine
Adenosine A2A Receptors
2-Amino-5-phosphonovalerate
Adenosine A1 Receptors
Chemical activation
Adenosine-5'-(N-ethylcarboxamide)
Microdialysis
Dopamine Receptors
Glutamate Receptors

Keywords

  • Adenosine
  • Caffeine
  • Dopamine
  • Glutamate
  • Microdialysis
  • NMDA receptor
  • Nucleus accumbens

ASJC Scopus subject areas

  • Biochemistry
  • Cellular and Molecular Neuroscience

Cite this

Adenosine receptor-mediated modulation of dopamine release in the nucleus accumbens depends on glutamate neurotransmission and N-methyl-D-aspartate receptor stimulation. / Quarta, Davide; Borycz, Janusz; Solinas, Marcello; Patkar, Kshitij; Hockemeyer, Jörg; Ciruela, Francisco; Lluis, Carme; Franco, Rafael; Woods, Amina S.; Goldberg, Steven R.; Ferré, Sergi.

In: Journal of Neurochemistry, Vol. 91, No. 4, 11.2004, p. 873-880.

Research output: Contribution to journalArticle

Quarta, D, Borycz, J, Solinas, M, Patkar, K, Hockemeyer, J, Ciruela, F, Lluis, C, Franco, R, Woods, AS, Goldberg, SR & Ferré, S 2004, 'Adenosine receptor-mediated modulation of dopamine release in the nucleus accumbens depends on glutamate neurotransmission and N-methyl-D-aspartate receptor stimulation', Journal of Neurochemistry, vol. 91, no. 4, pp. 873-880. https://doi.org/10.1111/j.1471-4159.2004.02761.x
Quarta, Davide ; Borycz, Janusz ; Solinas, Marcello ; Patkar, Kshitij ; Hockemeyer, Jörg ; Ciruela, Francisco ; Lluis, Carme ; Franco, Rafael ; Woods, Amina S. ; Goldberg, Steven R. ; Ferré, Sergi. / Adenosine receptor-mediated modulation of dopamine release in the nucleus accumbens depends on glutamate neurotransmission and N-methyl-D-aspartate receptor stimulation. In: Journal of Neurochemistry. 2004 ; Vol. 91, No. 4. pp. 873-880.
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AU - Hockemeyer, Jörg

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