Actions of cocaine on rat dopaminergic neurones in vitro (original) (raw)

Abstract

1. Intracellular recordings were made from neurones in vitro in the rat substantia nigra zona compacta and ventral tegmental area; the neurones had the characteristic properties of dopamine-containing cells, and fired action potentials spontaneously. 2. Cocaine (1-10 microM) inhibited spontaneous firing, hyperpolarized the membrane and (in neurones voltage-clamped at -60 mV) caused an outward membrane current; the minimally effective concentration was 1 microM. These effects were blocked by sulpiride (30 nM-1 microM). 3. Dopamine (3-100 microM) also inhibited firing, hyperpolarized and caused an outward current. These effects of dopamine were potentiated about five fold by cocaine (10 microM). 4. It is concluded that cocaine (1-10 microM) inhibits the firing and hyperpolarizes substantia nigra zona compacta neurones in vitro by blocking the uptake of dopamine which the cells continuously release.

731

Selected References

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

  1. Bonnet J. J., Protais P., Chagraoui A., Costentin J. High-affinity [3H]GBR 12783 binding to a specific site associated with the neuronal dopamine uptake complex in the central nervous system. Eur J Pharmacol. 1986 Jul 31;126(3):211–222. doi: 10.1016/0014-2999(86)90050-6. [DOI] [PubMed] [Google Scholar]
  2. Bunney B. S., Aghajanian G. K., Roth R. H. Comparison of effects of L-dopa, amphetamine and apomorphine on firing rate of rat dopaminergic neurones. Nat New Biol. 1973 Sep 26;245(143):123–125. doi: 10.1038/newbio245123a0. [DOI] [PubMed] [Google Scholar]
  3. Church W. H., Justice J. B., Jr, Neill D. B. Detecting behaviorally relevant changes in extracellular dopamine with microdialysis. Brain Res. 1987 Jun 2;412(2):397–399. doi: 10.1016/0006-8993(87)91150-4. [DOI] [PubMed] [Google Scholar]
  4. Di Chiara G., Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5274–5278. doi: 10.1073/pnas.85.14.5274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Einhorn L. C., Johansen P. A., White F. J. Electrophysiological effects of cocaine in the mesoaccumbens dopamine system: studies in the ventral tegmental area. J Neurosci. 1988 Jan;8(1):100–112. doi: 10.1523/JNEUROSCI.08-01-00100.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fibiger H. C. Drugs and reinforcement mechanisms: a critical review of the catecholamine theory. Annu Rev Pharmacol Toxicol. 1978;18:37–56. doi: 10.1146/annurev.pa.18.040178.000345. [DOI] [PubMed] [Google Scholar]
  7. Grace A. A., Bunney B. S. Intracellular and extracellular electrophysiology of nigral dopaminergic neurons--2. Action potential generating mechanisms and morphological correlates. Neuroscience. 1983 Oct;10(2):317–331. doi: 10.1016/0306-4522(83)90136-7. [DOI] [PubMed] [Google Scholar]
  8. Groves P. M., Wilson C. J., Young S. J., Rebec G. V. Self-inhibition by dopaminergic neurons. Science. 1975 Nov 7;190(4214):522–528. doi: 10.1126/science.242074. [DOI] [PubMed] [Google Scholar]
  9. Hadfield M. G., Nugent E. A. Cocaine: comparative effect on dopamine uptake in extrapyramidal and limbic systems. Biochem Pharmacol. 1983 Feb 15;32(4):744–746. doi: 10.1016/0006-2952(83)90509-9. [DOI] [PubMed] [Google Scholar]
  10. Heikkila R. E., Orlansky H., Cohen G. Studies on the distinction between uptake inhibition and release of (3H)dopamine in rat brain tissue slices. Biochem Pharmacol. 1975 Apr 15;24(8):847–852. doi: 10.1016/0006-2952(75)90152-5. [DOI] [PubMed] [Google Scholar]
  11. Higashi H., Inanaga K., Nishi S., Uchimura N. Enhancement of dopamine actions on rat nucleus accumbens neurones in vitro after methamphetamine pre-treatment. J Physiol. 1989 Jan;408:587–603. doi: 10.1113/jphysiol.1989.sp017478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Javaid J. I., Fischman M. W., Schuster C. R., Dekirmenjian H., Davis J. M. Cocaine plasma concentration: relation to physiological and subjective effects in humans. Science. 1978 Oct 13;202(4364):227–228. doi: 10.1126/science.694530. [DOI] [PubMed] [Google Scholar]
  13. Kennedy L. T., Hanbauer I. Sodium-sensitive cocaine binding to rat striatal membrane: possible relationship to dopamine uptake sites. J Neurochem. 1983 Jul;41(1):172–178. doi: 10.1111/j.1471-4159.1983.tb13666.x. [DOI] [PubMed] [Google Scholar]
  14. Koob G. F., Bloom F. E. Cellular and molecular mechanisms of drug dependence. Science. 1988 Nov 4;242(4879):715–723. doi: 10.1126/science.2903550. [DOI] [PubMed] [Google Scholar]
  15. Lacey M. G., Mercuri N. B., North R. A. Dopamine acts on D2 receptors to increase potassium conductance in neurones of the rat substantia nigra zona compacta. J Physiol. 1987 Nov;392:397–416. doi: 10.1113/jphysiol.1987.sp016787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lacey M. G., Mercuri N. B., North R. A. On the potassium conductance increase activated by GABAB and dopamine D2 receptors in rat substantia nigra neurones. J Physiol. 1988 Jul;401:437–453. doi: 10.1113/jphysiol.1988.sp017171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lacey M. G., Mercuri N. B., North R. A. Two cell types in rat substantia nigra zona compacta distinguished by membrane properties and the actions of dopamine and opioids. J Neurosci. 1989 Apr;9(4):1233–1241. doi: 10.1523/JNEUROSCI.09-04-01233.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Missale C., Castelletti L., Govoni S., Spano P. F., Trabucchi M., Hanbauer I. Dopamine uptake is differentially regulated in rat striatum and nucleus accumbens. J Neurochem. 1985 Jul;45(1):51–56. doi: 10.1111/j.1471-4159.1985.tb05473.x. [DOI] [PubMed] [Google Scholar]
  19. Nicolaysen L. C., Pan H. T., Justice J. B., Jr Extracellular cocaine and dopamine concentrations are linearly related in rat striatum. Brain Res. 1988 Jul 26;456(2):317–323. doi: 10.1016/0006-8993(88)90234-x. [DOI] [PubMed] [Google Scholar]
  20. Pan Z. Z., Williams J. T. Differential actions of cocaine and amphetamine on dorsal raphe neurons in vitro. J Pharmacol Exp Ther. 1989 Oct;251(1):56–62. [PubMed] [Google Scholar]
  21. Ritz M. C., Lamb R. J., Goldberg S. R., Kuhar M. J. Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science. 1987 Sep 4;237(4819):1219–1223. doi: 10.1126/science.2820058. [DOI] [PubMed] [Google Scholar]
  22. Roberts D. C., Koob G. F. Disruption of cocaine self-administration following 6-hydroxydopamine lesions of the ventral tegmental area in rats. Pharmacol Biochem Behav. 1982 Nov;17(5):901–904. doi: 10.1016/0091-3057(82)90469-5. [DOI] [PubMed] [Google Scholar]
  23. Schoemaker H., Pimoule C., Arbilla S., Scatton B., Javoy-Agid F., Langer S. Z. Sodium dependent [3H]cocaine binding associated with dopamine uptake sites in the rat striatum and human putamen decrease after dopaminergic denervation and in Parkinsons disease. Naunyn Schmiedebergs Arch Pharmacol. 1985 May;329(3):227–235. doi: 10.1007/BF00501873. [DOI] [PubMed] [Google Scholar]
  24. Starke K. Presynaptic receptors. Annu Rev Pharmacol Toxicol. 1981;21:7–30. doi: 10.1146/annurev.pa.21.040181.000255. [DOI] [PubMed] [Google Scholar]
  25. Surprenant A., Williams J. T. Inhibitory synaptic potentials recorded from mammalian neurones prolonged by blockade of noradrenaline uptake. J Physiol. 1987 Jan;382:87–103. doi: 10.1113/jphysiol.1987.sp016357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tagerud S. E., Cuello A. C. Dopamine release from the rat substantia nigra in vitro. Effect of raphe lesions and veratridine stimulation. Neuroscience. 1979;4(12):2021–2029. doi: 10.1016/0306-4522(79)90073-3. [DOI] [PubMed] [Google Scholar]
  27. Uchimura N., Higashi H., Nishi S. Hyperpolarizing and depolarizing actions of dopamine via D-1 and D-2 receptors on nucleus accumbens neurons. Brain Res. 1986 Jun 11;375(2):368–372. doi: 10.1016/0006-8993(86)90760-2. [DOI] [PubMed] [Google Scholar]
  28. Uchimura N., North R. A. Actions of cocaine on rat nucleus accumbens neurones in vitro. Br J Pharmacol. 1990 Apr;99(4):736–740. doi: 10.1111/j.1476-5381.1990.tb12999.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. White F. J., Wang R. Y. Electrophysiological evidence for the existence of both D-1 and D-2 dopamine receptors in the rat nucleus accumbens. J Neurosci. 1986 Jan;6(1):274–280. doi: 10.1523/JNEUROSCI.06-01-00274.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Williams J., Lacey M. Actions of cocaine on central monoamine neurons: intracellular recordings in vitro. NIDA Res Monogr. 1988;90:234–242. [PubMed] [Google Scholar]
  31. Wise R. A. Neural mechanisms of the reinforcing action of cocaine. NIDA Res Monogr. 1984;50:15–33. [PubMed] [Google Scholar]
  32. Woodruff G. N., McCarthy P. S., Walker R. J. Studies on the pharmacology of neurones in the nucleus accumbens of the rat. Brain Res. 1976 Oct 15;115(2):233–242. doi: 10.1016/0006-8993(76)90509-6. [DOI] [PubMed] [Google Scholar]