Involvement of the corticostriatal glutamatergic pathway in ethanol-induced ascorbic acid release in rat striatum
JING LIU
Department of Pharmacology of Chinese Materia Medica, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang 110015, PR China
Search for more papers by this authorCorresponding Author
CHUN-FU WU
Department of Pharmacology of Chinese Materia Medica, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang 110015, PR China
Chun-Fu Wu, Department of Pharmacology of Chinese Materia Medica, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang 110015, PR China. Tel: + 86 24 23903205; Fax: + 86 24 23896050; e-mail: [email protected]Search for more papers by this authorWEN LIU
Department of Pharmacology of Chinese Materia Medica, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang 110015, PR China
Search for more papers by this authorHONG-LING ZHANG
Department of Pharmacology of Chinese Materia Medica, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang 110015, PR China
Search for more papers by this authorCHUN-LI LI
Department of Pharmacology of Chinese Materia Medica, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang 110015, PR China
Search for more papers by this authorJING LIU
Department of Pharmacology of Chinese Materia Medica, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang 110015, PR China
Search for more papers by this authorCorresponding Author
CHUN-FU WU
Department of Pharmacology of Chinese Materia Medica, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang 110015, PR China
Chun-Fu Wu, Department of Pharmacology of Chinese Materia Medica, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang 110015, PR China. Tel: + 86 24 23903205; Fax: + 86 24 23896050; e-mail: [email protected]Search for more papers by this authorWEN LIU
Department of Pharmacology of Chinese Materia Medica, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang 110015, PR China
Search for more papers by this authorHONG-LING ZHANG
Department of Pharmacology of Chinese Materia Medica, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang 110015, PR China
Search for more papers by this authorCHUN-LI LI
Department of Pharmacology of Chinese Materia Medica, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang 110015, PR China
Search for more papers by this authorAbstract
The mechanism of ethanol-induced ascorbic acid (AA) release in striatum is not well understood. In the present work, the possible involvement of NMDA receptors in the corticostriatal pathway was studied by microdialysis coupled to high performance liquid chromatography with electrochemical detection. Ethanol (3.0 g/kg i.p.) stimulated significant striatal AA release to more than 200% above the baseline. This effect of ethanol could be partially antagonized by amantadine, a non-selective NMDA receptor antagonist and dopamine releaser, at a dose of 200 mg/kg i.p. and significantly antagonized by MK-801, a non-competitive NMDA receptor antagonist, at the doses of 0.5 and 1.0 mg/kg i.p. Furthermore, deafferentation of the glutamatergic projection from cortex to striatum by undercutting the prefrontal cortex completely eliminated ethanol-induced AA release in rat striatum. The basal level of AA in striatum could only be reduced by high doses of MK-801, but not by low doses of MK-801, amantadine or decortication. The results further confirm that NMDA receptors are involved in ethanol-induced AA release and provide the first evidence for the necessity of the activation of corticostriatal glutamatergic pathway in ethanol-induced AA release in rat striatum.
References
- 1 Grunewald RA. Ascorbic acid in the brain. Brain Res Rev 1993; 18: 123–33.
- 2 Rebec GV, Pierce RC. A vitamin as neuromodulator: ascorbic acid release into the extracellular fluid of the brain regulates dopaminergic and glutamatergic transmission. Prog Neurobiol 1994; 43: 537–65.
- 3 Kayaalp SO, Rubenstein JS, Neff NE. Inhibition of dopamine D-1 and D-2 binding sites in neuronal tissue by ascorbate. Neuropharmacology 1981; 30: 409–10.
- 4 Cheng N, Maeda T, Kume T et al. Differential neurotoxicity induced by l-DOPA and dopamine in cultured striatal neurons. Brain Res 1996; 743: 278–83.
- 5 Majewska MD, Bell JA. Ascorbic acid protects neurons from injury induced by glutamate and NMDA. Neuroreport 1990; 1: 194–6.
- 6 Bell JA, Beglan CL, London ED. Interaction of ascorbic acid with the neurotoxic effects of NMDA and sodium nitroprusside. Life Sci 1995; 58: 367–71.
- 7 De Angelis L. Ascorbic acid and atypical antipsychotic drugs: modulation of amineptine-induced behaviour in mice. Brain Res 1995; 670: 303–7.
- 8 Dorris RL, Dill RE. Potentiation of haloperidol-induced catalepsy by ascorbic acid in rats and nonhuman primates. Pharmacol Biochem Behav 1986; 24: 781–3.
- 9 Ferko FP. Effect of L-ascorbic acid on ethanol-induced central nervous system depression in mice. Pharmacol Biochem Behav 1986; 24: 543–7.
- 10 Zetterstrom T, Sharp T, Marsden CA, Ungerstedt U. In vivo measurement of dopamine and its metabolites by intracerebral dialysis: changes after d-amphetamine. J Neurochem 1983; 41: 1769–73.
- 11 Wu CF, Liu W, Liu J, Yeh CH dl-Fenfluramine inhibits ethanol-induced ascorbic acid release in rat striatum studied by microdialysis. Addict Biol 1998; 3: 295–308.
- 12 O'Neill RD, Fillenz M, Albery WJ. Circadian changes in homovanillic acid and ascorbate levels in the rat striatum using microprocessor-controlled voltammetry. Neurosci Lett 1982; 34: 189–193.
- 13 Pierce RC, Rebec GV. Stimulation of both D[sub 1] and D[sub 2] receptors increases behavioral activation and ascorbate release in the neostriatum of freely moving rats. Eur J Pharmacol 1990; 191: 295–302.
- 14 Pierce RC, Clemens AJ, Shapiro LA, Rebec GV. Repeated treatment with ascorbate or haloperidol, but not clozapine, elevates extracellular ascorbate in the neostriatum of freely moving rats. Psychopharmacogy 1994; 116: 103–9.
- 15 Wu CP. Possible role of glutamatergic neurotransmission in regulating ethanol-evoked brain ascorbate release. Neurosci Lett 1994; 171: 105–8.
- 16 Wilson RL, Wightman RM. Systemic and nigral application of amphetamine both cause an increase in extracellular concentration of ascorbate in the caudate nucleus of the rat. Brain Res 1985; 339: 219–26.
- 17 Basse-Tomusk A, Rebec GV. Corticostriatal and thalamic regulation of amphetamine-induced ascorbate release in the neostriatum. Pharmacol Biochem Behav 1990; 35: 55–60.
- 18 Saponjic RM, Mueller K, Krug D, Kunko PM. The effects of haloperidol, scopolamine, and MK-801 on amphetamine-induced increases in ascorbic acid and uric acid as determined by voltammetry in vivo. Pharmacol Biochem Behav 1994; 48: 161–8.
- 19 Brazell MP, Mitchell SN, Joseph MH, Gray JA. Acute administration of nicotine increases the in vivo extracellular levels of dopamine, 3,4-dihydroxyphenylacetic acid and ascorbic acid preferentially in the nucleus accumbens of the rat: comparison with caudate-putamen. Neuropharmacology 1990; 29: 1177–85.
- 20 Enrico P, Esposito G, Mura MA et al. Effect of morphine on striatal dopamine metabolism and ascorbic acid and uric acid release in freely moving rats. Brain Res 1997; 745: 173–82.
- 21 Crespi F, Keane PE. The effect of diazepam and RO 15-1788 on extracellular ascorbic acid, DOPAC and 5-HIAA in striatum of anesthetized and conscious freely moving rats, as measured by differential pulse voltammetry. Neurosci Res 1987; 4: 323–41.
- 22 O'Neill RD, Fillenz M, Sundstrom L, Rawlins JNP. Voltammetrically monitored brain ascorbate as an index of excitatory amino acid release in the unrestrained rat. Neurosci Lett 1984; 52: 227–33.
- 23 Pierce RC, Rebec GV. Intraneostriatal administration of glutamate antagonists increases behavioral activation and decreases neostriatal ascorbate via nondopaminergic mechanisms. J Neurosci 1993; 13: 4272–80.
- 24 Oh C, Gardiner TV, Rebec GV. Blockade of both D[sub 1]- and D[sub 2]-dopamine receptors inhibits amphetamine-induced ascorbate release in the neostriatum. Brain Res 1989; 480: 184–9.
- 25 Wu CF, Liu J, Consolo S, Liu W. 5-HT[sub 1A] receptors mediate inhibition of ethanol-induced ascorbic acid release in rat striatum studied by microdialysis. Neurosci Lett 1998; 250: 95–8.
- 26 Desole MS, Miele M, Enrico P et al. Effects of cortical ablation on apomorphine-and scopolamine-induced changes in dopamine turnover and ascorbic acid catabolism in the rat striatum. Eur J Pharmacol 1992; 219: 67–74.
- 27 Miele M, Enrico P, Esposito G et al. Cortical ablation and drug-induced changes in striatal ascorbic acid oxidation and behavior in the rat. Pharmacol Biochem Behav 1995; 50: 1–7.
- 28 Murphy JM, Cunningham SD, McBride WJ. Effects of 250 mg% ethanol on monoamine and amino acid release from rat striatal slices. Brain Res Bull 1985; 14: 439–42.
- 29 McBride WJ, Murphy JM, Lumeng L, LI T-K. Effects of ethanol on monoamine and amino acid release from cerebral cortical slices of the alcohol-preferring P line of rats. Alcohol Clin Exp Res 1986; 10: 205–8.
- 30 Nie Z, Madamba SG, Siggins GR. Ethanol inhibits gluatamatergic neurotransmission in nucleus accumbens neurons by multiple mechanisms. J Pharmacol Exp Ther 1994; 271: 1566–73.
- 31 Caboni S, Isola R, Gessa G, Rossetti ZL. Ethanol prevents the glutamate release induced by N-methyl-D-aspartate in the rat striatum. Neurosci Lett 1993; 152: 133–6.
- 32 Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. Sydney : Academic Press; 1982.
- 33 Consolo S, Wu CF, Fiorentini F, Ladinsky H, Vezzani A. Determination of endogenous acetylcholine release in freely moving rats by transstriatal dialysis coupled to a radioenzymatic assay: effect of drugs. J Neurochem 1987; 48: 1459–65.
- 34 Wu CF, Bertorelli R, Sacconi M, Pepeu G, Consolo S. Decrease of brain acetylcholine release in aging freely moving rats detected by microdialysis. Neurobiol Aging 1988; 9: 357–61.
- 35 Consolo S, Sieklucka M, Fiorentini F, Forloni G, Ladinsky H. Frontal decortication and adaptive changes in striatal cholinergic neurons in the rats. Brain Res 1986; 363: 128–34.
- 36 Frye GD, Breese GR. GABAergic modulation of ethanol-induced motor impairment. J Pharmacol Exp Ther 1982; 223: 750–6.
- 37 Nurmi M, Kiianmaa K, Sinclair JD. Brain ethanol in AA, ANA, and Wistar rats monitored with one-minute microdialysis. Alcohol 1994; 11: 315–21.
- 38 Ferraro TN, Weyers P, Carrozza DP, Vogel WH. Continuous monitoring of brain ethanol levels by intracerebral microdialysis. Alcohol 1990; 7: 129–32.
- 39 Svensson L, Wu CP, Johannessen K, Engel JA. Effects of ethanol on ascorbate release in the nucleus accumbens and striatum of freely moving rats. Alcohol 1992; 9: 535–40.
- 40 Ghasemzadeh B, Cammack J, Adams RN. Dynamic changes in extracellular fluid ascorbic acid monitored by in vivo electrochemistry. Brain Res 1991; 547: 162–6.
- 41 Miele M, Boutelle MG, Fillenz M. The physiologically induced release of ascorbate in rat brain is dependent on impulse traffic, calcium influx and glutamate uptake. Neuroscience 1994; 62: 87–91.
- 42 Cammack J, Ghasemzadeh B, Adams RN. The pharmacological profile of glutamate-evoked ascorbic acid efflux measured by in vivo electrochemistry. Brain Res 1991; 565: 17–22.
- 43 Wu C. NMDA receptor antagonist CPP inhibits ethanol-evoked ascorbate release in the brain of freely moving rats. Neuro sci Lett 1993; 157: 111–14.
- 44 Wu CF, Liu W, Xu NJ, Liu J. Reserpine does not block ethanol-induced striatal ascorbate release in rats. Chinese J Neurosci 1995;(suppl), 33 (abstract).
- 45 Desole MS, Miele M, Enrico P et al. The effects of cortical ablation on d-amphetamine-induced changes in striatal dopamine turnover and ascorbic acid catabolism in the rat. Neurosci Lett 1992; 139: 29–33.
- 46 Rice ME, Russo-Menna I. Differential compartmentalization of brain ascorbate and glutathione between neurons and glia. Neuroscience 1998; 82: 1213–23.
- 47 Kim J-S, Hassler R, Haug P, Paik K-S. Effect of frontal cortex ablation on striatal glutamic acid level in rat. Brain Res 1977; 132: 370–74.
- 48 Hassler R, Haug P, Nitch C, Kim J-S, Paik K-S. Effect of motor and premotor cortex ablation on concentrations of amino acids, monoammines and acetylcholine and on the ultrastructure in rat striatum. A confirmation of glutamate as the specific corticostriatal transmitter. J Neurochem 1982; 38: 1087–98.
- 49 Warenycia MW, McKenzie GM, Murphy M, Szerb JC. The effects of cortical ablation on multiple unit activity in the striatum following dexamphetamine. Neuropharmacology 1987; 26: 1107–14.
- 50 Shenk JO, Miller E, Gaddis E, Adams RN. Homeostatic control of ascorbate concentration in CNS extracellular fluid. Brain Res 1982; 253: 353–56.
- 51 Mizoguchi K, Yokoo M, Yoshida Tanaka T, Tanaka M. Amantadine increases the extracellular dopamine levels in the striatum by re-uptake inhibition and by N-methyl-D-aspartate antagonism. Brain Res 1994; 662: 255–8.
- 52 Kornhuber J, Bormann J, Huebers M, Rusche K, Riederer P. Effects of the 1-amino-adamantanes at the MK-801-binding site of the NMDA-receptorgated ion channel: a human postmortem brain. Eur J Pharmacol 1991; 206: 297–300.
- 53 Stoof JC, Booij J, Drukarch B, Wolters EC. The antiparkinsonian drug amantadine inhibits the N-methyl-D-aspartic acid-evoked release of acetylcholine from rat neostriatum in a noncompetitive way. Eur J Pharmacol 1992; 213: 439–43.
- 54 Verge D, Daval G, Marcinkiewicz M et al. Quantitative autoradiography of multiple 5-HT[sub 1] receptor subtypes in the brain of control or 5,7-dihyroxytryptamine-treated rats. J Neurosci 1986; 6: 3474–82.