Summary
Dopamine (DA) release from nerve terminals of the nigrostriatal DA neurons not only depends on the activity of nigral DA cells but also on presynaptic regulation. Glutamatergie neurons of cortical origin play a prominent role in these presynaptic regulations. The direct glutamatergic presynaptic control of DA release is mediated by N-methyl-D-aspartate (NMDA) andα-amino-3-hydroxy-5-methyl-4-isoxazole-4-propionate (AMPA) receptors, located on DA nerve terminals. In addition, by acting on striatal target cells, these glutamatergic neurons contribute also to indirect regulations of DA release involving several transmitters such as GABA, acetylcholine and neuropeptides. Diffusible messengers such as nitric oxide (NO) or arachidonic acid (AA) which are particularly formed under the stimulation of NMDA receptors may also participate to the regulation of DA release. In the present study, it will be shown that the co-application of NMDA and carbachol synergistically increases the release of [3H]-DA and that this effect is reduced by mepacrine or 4-bromophenacylbromide (107M), two inhibitors of PLA2. Therefore endogenously released AA induced by the co-stimulation of NMDA and cholinergic receptors seems to be involved, at least partly, in the release of DA.
Similar content being viewed by others
References
Carter CJ, L'Heureux R, Scatton B (1988) Differential control by N-methyl-D-aspartate and kainate of striatal dopamine releasein vivo: a trans-striatal dialysis study. J Neurochem 51: 462–468
Chen L, Huang LYM (1992) Protein kinase C reduces Mg−+ block of NMDA receptor channels as a mechanism of modulation. Nature 356: 521–523
Chéramy A, Romo R, Godeheu G, Baruch P, Glowinski J (1986)In vivo presynaptic control of dopamine release in the cat caudate nucleus II. Facilitatory or inhibitory influence of L-glutamate. Neuroscience 19: 1081–1090
Chéramy A, Kernel ML, Gauchy C, Desce JM, Barbeito L, Glowinski J (1991) Role of excitatory amino acids in the direct and indirect presynaptic regulation of dopamine release from nerve terminals and dendrites of nigrostriatal dopaminergic neurons. Amino Acids 1: 351–363
Chéramy A, Godeheu G, L'hirondel M, Glowinski J (1996) Cooperative contributions of cholinergic and NMDA receptors in the presynaptic control of dopamine release from synaptosomes of the rat striatum. J Pharmacol Exp Ther 276: 616–625
Desce JM, Godeheu G, Galli T, Artaud F, Chéramy A, Glowinski J (1991) Presynaptic facilitation of dopamine release through AMPA receptors on synaptosomes from the rat striatum. J Pharmacol Exp Ther 259: 692–698
Desce JM, Godeheu G, Galli T, Artaud F, Chéramy A, Glowinski J (1992) L-glutamateevoked release of dopamine from synaptosomes of the rat striatum: involvement of AMPA and NMDA receptors. Neuroscience 47: 333–339
Giorguieff MF, Kernel ML, Glowinski J (1977a) Presynaptic effect of L-glutamic acid on the release of dopamine in rat striatal slices. Neurosci Lett 6: 73–77
Giorguieff MF, Le Floch ML, Glowinski J, Besson MJ (1977b) Involvement of cholinergic presynaptic receptors of nicotinic and muscarinic types in the control of the spontaneous release of dopamine from striatal dopaminergic terminals in the rat. J Pharmacol Exp Ther 200: 535–544
Hanbauer I, Wink D, Osawa Y, Edelman GM, Gally JA (1992) Role of nitric oxide in NMDA-evoked release of [3H]-dopamine from striatal slices. NeuroReport 3:409–412
Imperato A, Honoré T, Jensen LH (1990) Dopamine release in the nucleus caudatus and in the nucleus accumbens is under glutamatergic control through non-NMDA receptors: a study in freely-moving rats. Brain Res 530: 223–228
Keefe KA, Zigmond MJ, Abercrombie ED (1992) Extracellular dopamine in striatum: influence of nerve impulse activity in medial forebrain bundle and local glutamatergic input. Neuroscience 47: 325–332
Krebs MO, Gauchy C, Desban M, Glowinski J, Kernel ML (1994) Role of dynorphin and GABA in the inhibitory regulation of NMDA-induced dopamine release in striosome- and matrix-enriched areas of the rat striatum. J Neurosci 14: 2435–2443
L'hirondel M, Chéramy A, Godeheu G, Glowinski J (1995) Effects of arachidonic acid on dopamine synthesis, spontaneous release and uptake in striatal synaptosomes from the rat. J Neurochem 64: 1406–1409
Leviel V, Gobert A, Guibert B (1990) The glutamate-mediated release of dopamine in the rat striatum: further characterization of the dual excitatory-inhibitory function. Neuroscience 39: 305–312
Martin LJ, Blackstone CD, Levey AI, Huganir RL, Price DL (1993) AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience 53: 327–358
Mount H, Welner S, Quirion R, Boksa P (1989) Glutamate stimulation of 3H-Dopamine release from dissociated cell cultures of rat ventral mesencephalon. J Neurochem 52: 1300–1310
Rapier C, Lunt GG, Wonnacott S (1990) Nicotinic modulation of 3H-dopamine release from striatal synaptosomes: pharmacological characterisation. J Neurochem 54:937–945
Rudolph MI, Arqueros L, Bustos L (1983) L-glutamic acid, a neuromodulator of dopaminergic transmission in the rat corpus striatum. Neurochem Int 5: 479–486
Standaert DG, Testa CM, Young AB, Penney JB (1994) Organization of N-methyl-Daspartate glutamate receptor gene expression in the basal ganglia of the rat. J Comp Neurol 343: 1–16
Suaud-Chagny MF, Chergui K, Chouvet G, Gonon F (1992) Relationship between dopamine release in the rat nucleus accumbens and the discharge activity of dopaminergic neurons during localin vivo application of amino acids in the ventral tegmental area. Neuroscience 49: 63–72
Tencé M, Murphy NP, Cordier J, Prémont J, Glowinski J (1995) Synergistic effects of acetylcholine and glutamate on the release of arachidonic acid from cultured striatal neurons. J Neurochem 64: 1605–1613
Wang JK (1991) Presynaptic glutamate receptors modulate dopamine release from striatal synaptosomes. J Neurochem 57: 819–822
Wüllner U, Brouillet E, Isacson O, Young AB, Penney JB (1993) Glutamate receptor binding sites in MPTP-treated mice. Exp Neurol 121: 284–287
Wüllner U, Testa CM, Catania MV, Young AB, Penney JB (1994) Glutamate receptors in striatum and substantia nigra: effects of medial forebrain bundle lesions. Brain Res 645: 98–102
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Chéramy, A., L'hirondel, M., Godeheu, G. et al. Direct and indirect presynaptic control of dopamine release by excitatory amino acids. Amino Acids 14, 63–68 (1998). https://doi.org/10.1007/BF01345244
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01345244