Skip to main content
NCBI home page
British Journal of Pharmacology logoLink to British Journal of Pharmacology
. 1991 Sep;104(1):15–20. doi: 10.1111/j.1476-5381.1991.tb12377.x

Effect of acute and subchronic nicotine treatment on cortical efflux of [3H]-D-aspartate and endogenous GABA in freely moving guinea-pigs.

L Beani 1, S Tanganelli 1, T Antonelli 1, L Ferraro 1, M Morari 1, P Spalluto 1, A Nordberg 1, C Bianchi 1
PMCID: PMC1908294  PMID: 1664759

Abstract

1. The [3H]-D-aspartate preloading of the parietal cortex of freely moving guinea-pigs equipped with epidural cups makes it possible to investigate drug effects on the efflux of this radiolabel, assumed as a marker of the glutamatergic structures underlying the cup. In the same model, the efflux of [3H]-gamma-aminobutyric acid ([3H]-GABA) and endogenous GABA can be measured. 2. Nicotine, 0.9-3.6 mg kg-1, s.c., or 3-5 micrograms, i.c.v., increased the efflux of [3H]-D-aspartate but reduced that of GABA. 3. These effects were mediated through mecamylamine-sensitive receptors but the ganglionic blocking agent was devoid of any primary activity. 4. The inhibition of GABA efflux induced by nicotine 3.6 mg kg-1, s.c., was abolished by methysergide 2 mg kg-1, i.p. and was reduced by naloxone 3 mg kg-1, i.p. pretreatment, suggesting the involvement of tryptaminergic and opioid systems. In contrast, muscarinic and catecholamine antagonists were ineffective. 5. Chronic treatment with nicotine (3.6 mg kg-1, twice daily for 16 days) reduced the facilitatory effect of [3H]-D-aspartate and abolished the inhibition of endogenous GABA efflux. 6. A slight increase in the number of nicotinic binding sites (by use of [3H]-nicotine as ligand) was found in the neocortex of chronically treated guinea-pigs. 7. The higher degree of tolerance to chronic nicotine treatment shown by GABA as compared with [3H]-D-aspartate efflux suggests that adaptative changes of the inhibitory neuronal pools prevail. This may contribute to the reinforcing and addictive properties of nicotine.

Full text

PDF
15

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Antonelli T., Beani L., Bianchi C., Rando S., Simonato M., Tanganelli S. Cortical acetylcholine release is increased and gamma-aminobutyric acid outflow is reduced during morphine withdrawal. Br J Pharmacol. 1986 Dec;89(4):853–860. doi: 10.1111/j.1476-5381.1986.tb11191.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Austin M. C., Kalivas P. W. The effect of cholinergic stimulation in the nucleus accumbens on locomotor behavior. Brain Res. 1988 Feb 16;441(1-2):209–214. doi: 10.1016/0006-8993(88)91400-x. [DOI] [PubMed] [Google Scholar]
  3. Balfour D. J. The effects of nicotine on brain neurotransmitter systems. Pharmacol Ther. 1982;16(2):269–282. doi: 10.1016/0163-7258(82)90058-4. [DOI] [PubMed] [Google Scholar]
  4. Beani L., Bianchi C., Ferraro L., Nilsson L., Nordberg A., Romanelli L., Spalluto P., Sundwall A., Tanganelli S. Effect of nicotine on the release of acetylcholine and amino acids in the brain. Prog Brain Res. 1989;79:149–155. doi: 10.1016/s0079-6123(08)62474-7. [DOI] [PubMed] [Google Scholar]
  5. Beani L., Bianchi C., Santinoceto L., Marchetti P. The cerebral acetylcholine release in conscious rabbits with semi-permanently implanted epidural cups. Int J Neuropharmacol. 1968 Sep;7(5):469–481. doi: 10.1016/0028-3908(68)90046-4. [DOI] [PubMed] [Google Scholar]
  6. Beani L., Bianchi C., Tanganelli S., Antonelli T., Simonato M., Rando S. Inversion of the alpha-2 and alpha-1 noradrenergic control of the cortical release of acetylcholine and gamma-aminobutyric acid in morphine-tolerant guinea pigs. J Pharmacol Exp Ther. 1988 Oct;247(1):294–301. [PubMed] [Google Scholar]
  7. Brennan M. J., Cantrill R. C., Wylie B. A. Modulation of synaptosomal GABA release by enkephalin. Life Sci. 1980 Sep 22;27(12):1097–1101. doi: 10.1016/0024-3205(80)90035-1. [DOI] [PubMed] [Google Scholar]
  8. Clarke P. B. Dopaminergic mechanisms in the locomotor stimulant effects of nicotine. Biochem Pharmacol. 1990 Oct 1;40(7):1427–1432. doi: 10.1016/0006-2952(90)90436-o. [DOI] [PubMed] [Google Scholar]
  9. Clarke P. B., Kumar R. The effects of nicotine on locomotor activity in non-tolerant and tolerant rats. Br J Pharmacol. 1983 Feb;78(2):329–337. doi: 10.1111/j.1476-5381.1983.tb09398.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Davies L. P., Johnston G. A. Uptake and release of D- and L-aspartate by rat brain slices. J Neurochem. 1976 May;26(5):1007–1014. doi: 10.1111/j.1471-4159.1976.tb06485.x. [DOI] [PubMed] [Google Scholar]
  11. Dewar D., Jenner P., Marsden C. D. Effects of opioid agonist drugs on the in vitro release of 3H-GABA, 3H-dopamine and 3H-5HT from slices of rat globus pallidus. Biochem Pharmacol. 1987 May 15;36(10):1738–1741. doi: 10.1016/0006-2952(87)90062-1. [DOI] [PubMed] [Google Scholar]
  12. Egan T. M. Single cell studies of the actions of agonists and antagonists on nicotinic receptors of the central nervous system. Prog Brain Res. 1989;79:73–83. doi: 10.1016/s0079-6123(08)62466-8. [DOI] [PubMed] [Google Scholar]
  13. Freeman G. B., Sherman K. A., Gibson G. E. Locomotor activity as a predictor of times and dosages for studies of nicotine's neurochemical actions. Pharmacol Biochem Behav. 1987 Feb;26(2):305–312. doi: 10.1016/0091-3057(87)90123-7. [DOI] [PubMed] [Google Scholar]
  14. Freund R. K., Jungschaffer D. A., Collins A. C., Wehner J. M. Evidence for modulation of GABAergic neurotransmission by nicotine. Brain Res. 1988 Jun 21;453(1-2):215–220. doi: 10.1016/0006-8993(88)90160-6. [DOI] [PubMed] [Google Scholar]
  15. Grenhoff J., Svensson T. H. Pharmacology of nicotine. Br J Addict. 1989 May;84(5):477–492. doi: 10.1111/j.1360-0443.1989.tb00604.x. [DOI] [PubMed] [Google Scholar]
  16. Hajós M., Engberg G. Role of primary sensory neurons in the central effects of nicotine. Psychopharmacology (Berl) 1988;94(4):468–470. doi: 10.1007/BF00212839. [DOI] [PubMed] [Google Scholar]
  17. Imperato A., Mulas A., Di Chiara G. Nicotine preferentially stimulates dopamine release in the limbic system of freely moving rats. Eur J Pharmacol. 1986 Dec 16;132(2-3):337–338. doi: 10.1016/0014-2999(86)90629-1. [DOI] [PubMed] [Google Scholar]
  18. Limberger N., Späth L., Starke K. A search for receptors modulating the release of gamma-[3H]aminobutyric acid in rabbit caudate nucleus slices. J Neurochem. 1986 Apr;46(4):1109–1117. doi: 10.1111/j.1471-4159.1986.tb00625.x. [DOI] [PubMed] [Google Scholar]
  19. Marchi M., Besana E., Raiteri M. Oxiracetam increases the release of endogenous glutamate from depolarized rat hippocampal slices. Eur J Pharmacol. 1990 Aug 28;185(2-3):247–249. doi: 10.1016/0014-2999(90)90650-u. [DOI] [PubMed] [Google Scholar]
  20. Morrison C. F., Stephenson J. A. The occurrence of tolerance to a central depressant effect of nicotine. Br J Pharmacol. 1972 Sep;46(1):151–156. doi: 10.1111/j.1476-5381.1972.tb06857.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nielsen E. O., Aarslew-Jensen M., Diemer N. H., Krogsgaard-Larsen P., Schousboe A. Baclofen-induced, calcium-dependent stimulation of in vivo release of D-[3H]aspartate from rat hippocampus monitored by intracerebral microdialysis. Neurochem Res. 1989 Apr;14(4):321–326. doi: 10.1007/BF01000034. [DOI] [PubMed] [Google Scholar]
  22. Nordberg A., Romanelli L., Sundwall A., Bianchi C., Beani L. Effect of acute and subchronic nicotine treatment on cortical acetylcholine release and on nicotinic receptors in rats and guinea-pigs. Br J Pharmacol. 1989 Sep;98(1):71–78. doi: 10.1111/j.1476-5381.1989.tb16864.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pomerleau O. F. Nicotine as a psychoactive drug: anxiety and pain reduction. Psychopharmacol Bull. 1986;22(3):865–869. [PubMed] [Google Scholar]
  24. Pomerleau O. F., Pomerleau C. S. Neuroregulators and the reinforcement of smoking: towards a biobehavioral explanation. Neurosci Biobehav Rev. 1984 Winter;8(4):503–513. doi: 10.1016/0149-7634(84)90007-1. [DOI] [PubMed] [Google Scholar]
  25. Romanelli L., Ohman B., Adem A., Nordberg A. Subchronic treatment of rats with nicotine: interconversion of nicotinic receptor subtypes in brain. Eur J Pharmacol. 1988 Mar 29;148(2):289–291. doi: 10.1016/0014-2999(88)90577-8. [DOI] [PubMed] [Google Scholar]
  26. Russell M. A. Subjective and behavioural effects of nicotine in humans: some sources of individual variation. Prog Brain Res. 1989;79:289–302. doi: 10.1016/s0079-6123(08)62488-7. [DOI] [PubMed] [Google Scholar]
  27. Wonnacott S., Irons J., Rapier C., Thorne B., Lunt G. G. Presynaptic modulation of transmitter release by nicotinic receptors. Prog Brain Res. 1989;79:157–163. doi: 10.1016/s0079-6123(08)62475-9. [DOI] [PubMed] [Google Scholar]
  28. Wonnacott S. The paradox of nicotinic acetylcholine receptor upregulation by nicotine. Trends Pharmacol Sci. 1990 Jun;11(6):216–219. doi: 10.1016/0165-6147(90)90242-z. [DOI] [PubMed] [Google Scholar]
  29. Young A. M., Foley P. M., Bradford H. F. Preloading in vivo: a rapid and reliable method for measuring gamma-aminobutyric acid and glutamate fluxes by microdialysis. J Neurochem. 1990 Sep;55(3):1060–1063. doi: 10.1111/j.1471-4159.1990.tb04597.x. [DOI] [PubMed] [Google Scholar]
  30. de la Garza R., Bickford-Wimer P. C., Hoffer B. J., Freedman R. Heterogeneity of nicotine actions in the rat cerebellum: an in vivo electrophysiologic study. J Pharmacol Exp Ther. 1987 Feb;240(2):689–695. [PubMed] [Google Scholar]
  31. de la Garza R., Freedman R., Hoffer J. Nicotine-induced inhibition of cerebellar Purkinje neurons: specific actions of nicotine and selective blockade by mecamylamine. Neuropharmacology. 1989 May;28(5):495–501. doi: 10.1016/0028-3908(89)90085-3. [DOI] [PubMed] [Google Scholar]

Articles from British Journal of Pharmacology are provided here courtesy of The British Pharmacological Society

RESOURCES