Home LiteratureArticle Details
PMID: 9204911 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A postsynaptic interaction between dopamine D1 and NMDA receptors promotes presynaptic inhibition in the rat nucleus accumbens via adenosine release.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 17 ·No. 14 ·1997-07-15 ·Pages 5271-80

Harvey J, Lacey MG

Abstract

The mechanism underlying dopamine D1 receptor-mediated attenuation of glutamatergic synaptic input to nucleus accumbens (NAcc) neurons was investigated in slices of rat forebrain, using whole-cell patch-clamp recording. The depression by dopamine of EPSCs evoked by single-shock cortical stimulation was stimulus-dependent. Synaptic activation of NMDA-type glutamate receptors was critical for this effect, because dopamine-induced EPSC depressions were blocked by the competitive NMDA receptor antagonist D/L-2-amino-5-phosphonopentanoate (AP5). Application of NMDA also depressed the EPSC, and both this effect and the dopamine depressions were blocked by the A1 receptor antagonist 8-cyclopentyl-1,3-dipropylxanthine (DPCPX), implicating adenosine release in the EPSC depression. A1 receptor agonists also depressed EPSCs by a presynaptic action, causing increased paired-pulse facilitation, but this was insensitive to AP5. Activation of D1 receptors enhanced both postsynaptic inward currents evoked by NMDA application and the isolated NMDA receptor-mediated component of synaptic transmission. The biochemical processes underlying the dopamine-induced EPSC depression did not involve either protein kinase A or the production of cAMP and its metabolites, because this effect was resistant to the protein kinase inhibitors H89 and H7 and the cAMP-specific phosphodiesterase inhibitor rolipram. We conclude that activation of postsynaptic D1 receptors enhances the synaptic activation of NMDA receptors in nucleus accumbens neurons, thereby promoting a transsynaptic feedback inhibition of glutamatergic synaptic transmission via release of adenosine. Unusually for D1 receptors, this phenomenon occurs independently of adenylyl cyclase stimulation. This process may contribute to the locomotor stimulant action of dopaminergic agents in the NAcc.

MeSH Terms
2-Amino-5-phosphonovalerate/pharmacology Adenosine/metabolism Animals Dopamine/pharmacology Male Nucleus Accumbens/drug effects,physiology Rats Rats, Wistar Receptors, Dopamine D1/drug effects,physiology Receptors, N-Methyl-D-Aspartate/drug effects,physiology Synaptic Transmission/drug effects,physiology
Chemicals
Receptors, Dopamine D1 Receptors, N-Methyl-D-Aspartate 2-Amino-5-phosphonovalerate Adenosine Dopamine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Harvey J
Department of Pharmacology, The Medical School, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom.
Lacey M G
References (59)
59 references, click to expand
  1. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons.
    Science. 1990 Dec 7;250(4986):1429-32 PMID: 2147780
  2. Excitatory amino acid receptors mediate the orofacial stereotypy elicited by dopaminergic stimulation of the ventrolateral striatum.
    Neuroscience. 1994 May;60(1):85-95 PMID: 7914360
  3. Nitric oxide and synaptic function.
    Annu Rev Neurosci. 1994;17:153-83 PMID: 7516125
  4. Modulation of in vivo striatal transmitter release by nitric oxide and cyclic GMP.
    J Neurochem. 1994 Feb;62(2):807-10 PMID: 7905029
  5. mu-Opioid receptors modulate NMDA receptor-mediated responses in nucleus accumbens neurons.
    J Neurosci. 1997 Jan 1;17(1):11-22 PMID: 8987732
  6. Enhancement of NMDA responses by group I metabotropic glutamate receptor activation in striatal neurones.
    Br J Pharmacol. 1997 Mar;120(6):1007-14 PMID: 9134210
  7. The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data.
    Prog Neurobiol. 1994 Apr;42(6):719-61 PMID: 7938546
  8. Modulation of excitatory synaptic transmission by adenosine released from single hippocampal pyramidal neurons.
    J Neurosci. 1996 Sep 15;16(18):5603-12 PMID: 8795616
  9. Primary sequence of cyclic nucleotide phosphodiesterase isozymes and the design of selective inhibitors.
    Trends Pharmacol Sci. 1990 Apr;11(4):150-5 PMID: 2159198
  10. Nucleus accumbens NMDA antagonist decreases locomotor activity produced by cocaine, heroin or accumbens dopamine, but not caffeine.
    Pharmacol Biochem Behav. 1991 Dec;40(4):841-5 PMID: 1687766
  11. The inositol 1,4,5-trisphosphate pathway mediates cholinergic potentiation of rat hippocampal neuronal responses to NMDA.
    J Physiol. 1992 Feb;447:513-33 PMID: 1593457
  12. Presynaptic dopamine D1 receptors attenuate excitatory and inhibitory limbic inputs to the shell region of the rat nucleus accumbens studied in vitro.
    J Neurophysiol. 1992 May;67(5):1325-34 PMID: 1534574
  13. Endogenous and exogenous dopamine depress EPSCs in rat nucleus accumbens in vitro via D1 receptors activation.
    J Physiol. 1996 Apr 1;492 ( Pt 1):143-54 PMID: 8730590
  14. Activation of adenosine A1 receptors initiates short-term synaptic depression in rat striatum.
    Neurosci Lett. 1995 Oct 13;199(1):9-12 PMID: 8584233
  15. Characterization of metabotropic glutamate receptor-mediated facilitation of N-methyl-D-aspartate depolarization of neocortical neurones.
    Br J Pharmacol. 1996 Feb;117(4):675-83 PMID: 8646413
  16. The pharmacology and neural circuitry of sensitization to psychostimulants.
    Behav Pharmacol. 1993;4(4):315-334 PMID: 11224200
  17. Dopamine activation of the arachidonic acid cascade as a basis for D1/D2 receptor synergism.
    Nature. 1991 Sep 12;353(6340):164-7 PMID: 1909771
  18. Differential regulation of renal phospholipase C isoforms by catecholamines.
    J Clin Invest. 1995 Jan;95(1):304-8 PMID: 7814630
  19. Glutamate-dopamine interactions in the ventral striatum: role in locomotor activity and responding with conditioned reinforcement.
    Psychopharmacology (Berl). 1994 Aug;115(4):516-28 PMID: 7871097
  20. Pharmacological characterization of dopamine systems in the nucleus accumbens core and shell.
    Neuroscience. 1992;46(1):49-56 PMID: 1350665
  21. Potentiation of NMDA receptor currents by arachidonic acid.
    Nature. 1992 Feb 20;355(6362):722-5 PMID: 1371330
  22. Amphetamine and dopamine-induced immediate early gene expression in striatal neurons depends on postsynaptic NMDA receptors and calcium.
    J Neurosci. 1996 Jul 1;16(13):4231-9 PMID: 8753884
  23. Interactions between glutamatergic and monoaminergic systems within the basal ganglia--implications for schizophrenia and Parkinson's disease.
    Trends Neurosci. 1990 Jul;13(7):272-6 PMID: 1695402
  24. Neuromodulatory actions of dopamine in the neostriatum are dependent upon the excitatory amino acid receptor subtypes activated.
    Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9576-80 PMID: 7692449
  25. Expression of striatal D1 dopamine receptors coupled to inositol phosphate production and Ca2+ mobilization in Xenopus oocytes.
    Proc Natl Acad Sci U S A. 1990 Mar;87(6):2196-200 PMID: 1690425
  26. Evidence for the coupling of Gq protein to D1-like dopamine sites in rat striatum: possible role in dopamine-mediated inositol phosphate formation.
    Mol Pharmacol. 1995 Dec;48(6):988-94 PMID: 8848015
  27. Psychostimulants depress excitatory synaptic transmission in the nucleus accumbens via presynaptic D1-like dopamine receptors.
    J Neurosci. 1996 Mar 1;16(5):1591-604 PMID: 8774428
  28. Interactions between excitatory amino acids and dopamine systems in the forebrain: implications for schizophrenia and Parkinson's disease.
    Behav Pharmacol. 1995 Aug;6(5 And 6):478-491 PMID: 11224356
  29. Rewarding actions of phencyclidine and related drugs in nucleus accumbens shell and frontal cortex.
    J Neurosci. 1996 May 1;16(9):3112-22 PMID: 8622141
  30. Addiction to cocaine and amphetamine.
    Neuron. 1996 May;16(5):901-4 PMID: 8630246
  31. Excitatory synaptic transmission in neostriatal neurons: regulation by cyclic AMP-dependent mechanisms.
    J Neurosci. 1995 Mar;15(3 Pt 1):1704-13 PMID: 7891129
  32. Potentiation of cAMP responses by metabotropic glutamate receptors depresses excitatory synaptic transmission by a kinase-independent mechanism.
    Neuron. 1994 May;12(5):1121-9 PMID: 8185947
  33. Neurobiology of addiction.
    Curr Opin Neurobiol. 1996 Apr;6(2):243-51 PMID: 8725967
  34. 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. 1995 May 8;355(3):418-26 PMID: 7636023
  35. Electron microscopic analysis of D1 and D2 dopamine receptor proteins in the dorsal striatum and their synaptic relationships with motor corticostriatal afferents.
    J Neurosci. 1995 Jul;15(7 Pt 2):5222-37 PMID: 7623147
  36. Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex.
    J Neurosci Methods. 1989 Dec;30(3):203-10 PMID: 2607782
  37. cAMP-independent, G protein-linked inhibition of Na+/H+ exchange in renal brush border by D1 dopamine agonists.
    Am J Physiol. 1993 Jun;264(6 Pt 2):F1032-7 PMID: 8100686
  38. Signal transduction pathways involved in the acute potentiation of NMDA responses by 1S,3R-ACPD in rat hippocampal slices.
    Br J Pharmacol. 1993 Aug;109(4):1085-90 PMID: 8401919
  39. Non-synaptic release of ATP by electrical stimulation in slices of rat hippocampus, cerebellum and habenula.
    Eur J Neurosci. 1996 Jul;8(7):1510-5 PMID: 8758958
  40. Nitric oxide signaling in the central nervous system.
    Annu Rev Physiol. 1995;57:683-706 PMID: 7539993
  41. Opposing roles for D-1 and D-2 dopamine receptors in efflux of cyclic AMP from rat neostriatum.
    Nature. 1981 Nov 26;294(5839):366-8 PMID: 6273735
  42. Presynaptic dopamine-glutamate interactions in the nucleus accumbens regulate sensorimotor gating.
    Psychopharmacology (Berl). 1995 Aug;120(4):433-41 PMID: 8539324
  43. Neurobehavioural mechanisms of reward and motivation.
    Curr Opin Neurobiol. 1996 Apr;6(2):228-36 PMID: 8725965
  44. D1 dopamine receptor-mediated induction of zif268 and c-fos in the dopamine-depleted striatum: differential regulation and independence from NMDA receptors.
    J Comp Neurol. 1996 Apr 01;367(2):165-76 PMID: 8708002
  45. A common mechanism mediates long-term changes in synaptic transmission after chronic cocaine and morphine.
    Neuron. 1996 Mar;16(3):631-9 PMID: 8785060
  46. Release of adenosine by activation of NMDA receptors in the hippocampus.
    Science. 1994 Sep 30;265(5181):2098-101 PMID: 7916485
  47. Acute methamphetamine-induced zif/268, preprodynorphin, and preproenkephalin mRNA expression in rat striatum depends on activation of NMDA and kainate/AMPA receptors.
    Brain Res Bull. 1996;39(6):349-57 PMID: 9138744
  48. Modulatory actions of dopamine on NMDA receptor-mediated responses are reduced in D1A-deficient mutant mice.
    J Neurosci. 1996 Sep 15;16(18):5870-82 PMID: 8795639
  49. N-methyl-D-aspartate- and non-N-methyl-D-aspartate-evoked adenosine release from rat cortical slices: distinct purinergic sources and mechanisms of release.
    J Neurochem. 1993 Mar;60(3):1073-80 PMID: 7679722
  50. Purinoceptors in the nervous system.
    Pharmacol Toxicol. 1995 Apr;76(4):228-39 PMID: 7617551
  51. Drugs of abuse: anatomy, pharmacology and function of reward pathways.
    Trends Pharmacol Sci. 1992 May;13(5):177-84 PMID: 1604710
  52. Protein kinase C modulation of NMDA currents: an important link for LTP induction.
    Trends Neurosci. 1992 Sep;15(9):333-9 PMID: 1382331
  53. The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons.
    J Neurosci. 1996 Apr 1;16(7):2397-410 PMID: 8601819
  54. Dopamine induces neurite retraction in retinal horizontal cells via diacylglycerol and protein kinase C.
    Proc Natl Acad Sci U S A. 1990 Dec;87(24):9693-7 PMID: 2263620
  55. Dopamine D1 receptor-mediated facilitation of GABAergic neurotransmission in the rat strioentopenduncular pathway and its modulation by adenosine A1 receptor-mediated mechanisms.
    Eur J Neurosci. 1996 Jul;8(7):1545-53 PMID: 8758962
  56. Physiological and morphological properties of accumbens core and shell neurons recorded in vitro.
    Synapse. 1993 Feb;13(2):135-60 PMID: 8446922
  57. Baclofen and adenosine inhibit synaptic potentials mediated by gamma-aminobutyric acid and glutamate release in rat nucleus accumbens.
    J Pharmacol Exp Ther. 1991 Aug;258(2):663-8 PMID: 1678016
  58. Letter: Stimulation of locomotor activity following injection of dopamine into the nucleus accumbens.
    J Pharm Pharmacol. 1973 Dec;25(12):1003-5 PMID: 4150283
  59. Enhancement of dopamine actions on rat nucleus accumbens neurones in vitro after methamphetamine pre-treatment.
    J Physiol. 1989 Jan;408:587-603 PMID: 2550628
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1997-07-15
Pages
5271-80
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6793812
Subset
IM
External Links
PubMed source PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2