Chronic cocaine administration reduces striatal dopamine terminal density and striatal dopamine release which leads to drug-seeking behaviour

Neuroscience

Volumn 174, Issue , 2011, Pages 143-150

  Lee, J ^a   Parish, C L ^a   Tomas, D ^a   Horne, M K ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ST VINCENT S HOSPITAL   (Australia)

Author keywords

Addiction; Anti psychotic; Catecholamine; Cocaine; Dopamine transporter; In vivo microdialysis

Indexed keywords

COCAINE; DOPAMINE; DOPAMINE 2 RECEPTOR; DOPAMINE TRANSPORTER; HALOPERIDOL;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE RECEPTOR BLOCKING; DOPAMINE RELEASE; DOPAMINERGIC ACTIVITY; DOPAMINERGIC TRANSMISSION; DOSE RESPONSE; DRUG SEEKING BEHAVIOR; LONG TERM EXPOSURE; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; RISK REDUCTION;

ANIMALS; COCAINE; CORPUS STRIATUM; DOPAMINE; DRUG-SEEKING BEHAVIOR; HALOPERIDOL; MALE; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; RECEPTORS, DOPAMINE D2; SYNAPTIC TRANSMISSION;

EID: 78650939342     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.11.055     Document Type: Article

References (67)

1. Alleweireldt A.T., Weber S.M., Kirschner K.F., Bullock B.L., Neisewander J.L. Blockade or stimulation of D1 dopamine receptors attenuates cue reinstatement of extinguished cocaine-seeking behavior in rats. Psychopharmacology (Berl) 2002, 159:284-293.
2. Arbuthnott G.W., Fairbrother I.S., Butcher S.P. Brain microdialysis studies on the control of dopamine release and metabolism in vivo. J Neurosci Methods 1990, 34:73-81.
3. Beninger R.J., Miller R. Dopamine D1-like receptors and reward-related incentive learning. Neurosci Biobehav Rev 1998, 22:335-345.
4. Berke J.D., Hyman S.E. Addiction, dopamine, and the molecular mechanisms of memory. Neuron 2000, 25:515-532.
5. Bertran-Gonzalez J., Bosch C., Maroteaux M., Matamales M., Herve D., Valjent E., Girault J.A. Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci 2008, 28:5671-5685.
6. Bowyer J.F., Weiner N. Modulation of the Ca++-evoked release of [3H]dopamine from striatal synaptosomes by dopamine (D2) agonists and antagonists. J Pharmacol Exp Ther 1987, 241:27-33.
7. Calabresi P., Saiardi A., Pisani A., Baik J.H., Centonze D., Mercuri N.B., Bernardi G., Borrelli E. Abnormal synaptic plasticity in the striatum of mice lacking dopamine D2 receptors. J Neurosci 1997, 17:4536-4544.
8. Carlezon W.A., Thome J., Olson V.G., Lane-Ladd S.B., Brodkin E.S., Hiroi N., Duman R.S., Neve R.L., Nestler E.J. Regulation of cocaine reward by CREB. Science 1998, 282:2272-2275.
9. De Wit H., Wise R.A. Blockade of cocaine reinforcement in rats with the dopamine receptor blocker pimozide, but not with the noradrenergic blockers phentolamine or phenoxybenzamine. Can J Psychol 1977, 31:195-203.
10. Di Chiara G., Bassareo V. Reward system and addiction: what dopamine does and doesn't do. Curr Opin Pharmacol 2007, 7:69-76.
11. 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, 85:5274-5278.
12. Diana M., Pistis M., Carboni S., Gessa G.L., Rossetti Z.L. Profound decrement of mesolimbic dopaminergic neuronal activity during ethanol withdrawal syndrome in rats: electrophysiological and biochemical evidence. Proc Natl Acad Sci U S A 1993, 90:7966-7969.
13. Fairbrother I.S., Arbuthnott G.W., Kelly J.S., Butcher S.P. In vivo mechanisms underlying dopamine release from rat nigrostriatal terminals: I. Studies using veratrine and ouabain. J Neurochem 1990, 54:1834-1843.
14. Fairbrother I.S., Arbuthnott G.W., Kelly J.S., Butcher S.P. In vivo mechanisms underlying dopamine release from rat nigrostriatal terminals: II. Studies using potassium and tyramine. J Neurochem 1990, 54:1844-1851.
15. Fienberg A.A., Hiroi N., Mermelstein P.G., Song W., Snyder G.L., Nishi A., Cheramy A., O'Callaghan J.P., Miller D.B., Cole D.G., Corbett R., Haile C.N., Cooper D.C., Onn S.P., Grace A.A., Ouimet C.C., White F.J., Hyman S.E., Surmeier D.J., Girault J., Nestler E.J., Greengard P. DARPP-32: regulator of the efficacy of dopaminergic neurotransmission. Science 1998, 281:838-842.
16. Finkelstein D.I., Stanic D., Parish C.L., Drago J., Horne M.K. Quantified assessment of terminal density and innervation. Curr Protoc Neurosci 2004, Chapter 1: Unit 1.13.
17. Finkelstein D.I., Stanic D., Parish C.L., Tomas D., Dickson K., Horne M.K. Axonal sprouting following lesions of the rat substantia nigra. Neuroscience 2000, 97:99-112.
18. Gerdeman G.L., Partridge J.G., Lupica C.R., Lovinger D.M. It could be habit forming: drugs of abuse and striatal synaptic plasticity. Trends Neurosci 2003, 26:184-192.
19. Goto Y., Otani S., Grace A.A. The Yin and Yang of dopamine release: a new perspective. Neuropharmacology 2007, 53:583-587.
20. Gundersen H.J., Bagger P., Bendtsen T.F., Evans S.M., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., West M.J. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 1988, 96:857-881.
21. Hemby S.E., Smith J.E., Dworkin S.I. The effects of eticlopride and naltrexone on responding maintained by food, cocaine, heroin and cocaine/heroin combinations in rats. J Pharmacol Exp Ther 1996, 277:1247-1258.
22. Hiroi N., Brown J.R., Haile C.N., Ye H., Greenberg M.E., Nestler E.J. FosB mutant mice: loss of chronic cocaine induction of Fos-related proteins and heightened sensitivity to cocaine's psychomotor and rewarding effects. Proc Natl Acad Sci U S A 1997, 94:10397-10402.
23. Horne M.K., Lee J., Chen F., Lanning K., Tomas D., Lawrence A.J. Long-term administration of cocaine or serotonin reuptake inhibitors results in anatomical and neurochemical changes in noradrenergic, dopaminergic, and serotonin pathways. J Neurochem 2008, 106:1731-1744.
24. Howell L.L., Wilcox K.M., Lindsey K.P., Kimmel H.L. Olanzapine-induced suppression of cocaine self-administration in rhesus monkeys. Neuropsychopharmacology 2006, 31:585-593.
25. Hyman S.E., Malenka R.C., Nestler E.J. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 2006, 29:565-598.
26. Kalivas P.W., Duffy P. Effect of acute and daily cocaine treatment on extracellular dopamine in the nucleus accumbens. Synapse 1990, 5:48-58.
27. Khroyan T.V., Barrett-Larimore R.L., Rowlett J.K., Spealman R.D. Dopamine D1- and D2-like receptor mechanisms in relapse to cocaine-seeking behavior: effects of selective antagonists and agonists. J Pharmacol Exp Ther 2000, 294:680-687.
28. Koob G.F. The neurobiology of addiction: a neuroadaptational view relevant for diagnosis. Addiction 2006, 101(Suppl 1):23-30.
29. Koob G.F., Le Moal M. Addiction and the brain antireward system. Annu Rev Psychol 2008, 59:29-53.
30. Kuhar M.J., Ritz M.C., Boja J.W. The dopamine hypothesis of the reinforcing properties of cocaine. Trends Neurosci 1991, 14:299-302.
31. Kuhar M.J., Ritz M.C., Sharkey J. Cocaine receptors on dopamine transporters mediate cocaine-reinforced behavior. NIDA Res Monogr 1988, 88:14-22.
32. Lee J., Zhu W.M., Stanic D., Finkelstein D.I., Horne M.H., Henderson J., Lawrence A.J., O'Connor L., Tomas D., Drago J., Horne M.K. Sprouting of dopamine terminals and altered dopamine release and uptake in Parkinsonian dyskinaesia. Brain 2008, 131:1574-1587.
33. Lindgren N., Xu Z.Q., Herrera-Marschitz M., Haycock J., Hokfelt T., Fisone G. Dopamine D(2) receptors regulate tyrosine hydroxylase activity and phosphorylation at Ser40 in rat striatum. Eur J Neurosci 2001, 13:773-780.
34. Martinez D., Broft A., Foltin R.W., Slifstein M., Hwang D.R., Huang Y., Perez A., Frankle W.G., Cooper T., Kleber H.D., Fischman M.W., Laruelle M. Cocaine dependence and d2 receptor availability in the functional subdivisions of the striatum: relationship with cocaine-seeking behavior. Neuropsychopharmacology 2004, 29:1190-1202.
35. Martinez D., Narendran R., Foltin R.W., Slifstein M., Hwang D.R., Broft A., Huang Y., Cooper T.B., Fischman M.W., Kleber H.D., Laruelle M. Amphetamine-induced dopamine release: markedly blunted in cocaine dependence and predictive of the choice to self-administer cocaine. Am J Psychiatry 2007, 164:622-629.
36. Martinez D., Slifstein M., Narendran R., Foltin R.W., Broft A., Hwang D.R., Perez A., Abi-Dargham A., Fischman M.W., Kleber H.D., Laruelle M. Dopamine D1 receptors in cocaine dependence measured with PET and the choice to self-administer cocaine. Neuropsychopharmacology 2009, 34:1774-1782.
37. Missale C., Nash S.R., Robinson S.W., Jaber M., Caron M.G. Dopamine receptors: from structure to function. Physiol Rev 1998, 78:189-225.
38. Nader M.A., Morgan D., Gage H.D., Nader S.H., Calhoun T.L., Buchheimer N., Ehrenkaufer R., Mach R.H. PET imaging of dopamine D2 receptors during chronic cocaine self-administration in monkeys. Nat Neurosci 2006, 9:1050-1056.
39. Nestler E.J. Is there a common molecular pathway for addiction?. Nat Neurosci 2005, 8:1445-1449.
40. Nestler E.J. Review. Transcriptional mechanisms of addiction: role of DeltaFosB. Philos Trans R Soc Lond B Biol Sci 2008, 363:3245-3255.
41. Norrholm S.D., Bibb J.A., Nestler E.J., Ouimet C.C., Taylor J.R., Greengard P. Cocaine-induced proliferation of dendritic spines in nucleus accumbens is dependent on the activity of cyclin-dependent kinase-5. Neuroscience 2003, 116:19-22.
42. Parish C.L., Drago J., Stanic D., Borrelli E., Finkelstein D.I., Horne M.K. Haloperidol treatment reverses behavioural and anatomical changes in cocaine-dependent mice. Neurobiol Dis 2005, 19:301-311.
43. Parish C.L., Finkelstein D.I., Drago J., Borrelli E., Horne M.K. The role of dopamine receptors in regulating the size of axonal arbors. J Neurosci 2001, 21:5147-5157.
44. Parish C.L., Stanic D., Drago J., Borrelli E., Finkelstein D.I., Horne M.K. Effects of long-term treatment with dopamine receptor agonists and antagonists on terminal arbor size. Eur J Neurosci 2002, 16:787-794.
45. Picconi B., Pisani A., Centonze D., Battaglia G., Storto M., Nicoletti F., Bernardi G., Calabresi P. Striatal metabotropic glutamate receptor function following experimental parkinsonism and chronic levodopa treatment. Brain 2002, 125:2635-2645.
46. Robinson T.E., Kolb B. Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur J Neurosci 1999, 11:1598-1604.
47. Rossetti Z.L., Hmaidan Y., Gessa G.L. Marked inhibition of mesolimbic dopamine release: a common feature of ethanol, morphine, cocaine and amphetamine abstinence in rats. Eur J Pharmacol 1992, 221:227-234.
48. Rouge-Pont F., Usiello A., Benoit-Marand M., Gonon F., Piazza P.V., Borrelli E. Changes in extracellular dopamine induced by morphine and cocaine: crucial control by D2 receptors. J Neurosci 2002, 22:3293-3301.
49. Self D.W. Regulation of drug-taking and -seeking behaviors by neuroadaptations in the mesolimbic dopamine system. Neuropharmacology 2004, 47(Suppl 1):242-255.
50. Self D.W., Barnhart W.J., Lehman D.A., Nestler E.J. Opposite modulation of cocaine-seeking behavior by D1- and D2-like dopamine receptor agonists. Science 1996, 271:1586-1589.
51. Shen H.W., Toda S., Moussawi K., Bouknight A., Zahm D.S., Kalivas P.W. Altered dendritic spine plasticity in cocaine-withdrawn rats. J Neurosci 2009, 29:2876-2884.
52. Stanic D., Finkelstein D.I., Bourke D.W., Drago J., Horne M.K. Timecourse of striatal re-innervation following lesions of dopaminergic SNpc neurons of the rat. Eur J Neurosci 2003, 18:1175-1188.
53. Stanic D., Parish C.L., Zhu W.M., Krstew E.V., Lawrence A.J., Drago J., Finkelstein D.I., Horne M.K. Changes in function and ultrastructure of striatal dopaminergic terminals that regenerate following partial lesions of the SNpc. J Neurochem 2003, 86:329-343.
54. Tepper J.M., Nakamura S., Young S.J., Groves P.M. Autoreceptor-mediated changes in dopaminergic terminal excitability: effects of striatal drug infusions. Brain Res 1984, 309:317-333.
55. Tepper J.M., Sawyer S.F., Groves P.M. Electrophysiologically identified nigral dopaminergic neurons intracellularly labeled with HRP: light-microscopic analysis. J Neurosci 1987, 7:2794-2806.
56. Tepper J.M., Sun B.C., Martin L.P., Creese I. Functional roles of dopamine D2 and D3 autoreceptors on nigrostriatal neurons analyzed by antisense knockdown in vivo. J Neurosci 1997, 17:2519-2530.
57. Thomas M.J., Malenka R.C. Synaptic plasticity in the mesolimbic dopamine system. Philos Trans R Soc Lond B Biol Sci 2003, 358:815-819.
58. Valjent E., Corvol J.C., Pages C., Besson M.J., Maldonado R., Caboche J. Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. J Neurosci 2000, 20:8701-8709.
59. Valjent E., Pascoli V., Svenningsson P., Paul S., Enslen H., Corvol J.C., Stipanovich A., Caboche J., Lombroso P.J., Nairn A.C., Greengard P., Herve D., Girault J.A. Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc Natl Acad Sci U S A 2005, 102:491-496.
60. Volkow N.D., Fowler J.S., Wang G.J., Baler R., Telang F. Imaging dopamine's role in drug abuse and addiction. Neuropharmacology 2009, 56(Suppl 1):3-8.
61. Volkow N.D., Fowler J.S., Wang G.J., Hitzemann R., Logan J., Schlyer D.J., Dewey S.L., Wolf A.P. Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse 1993, 14:169-177.
62. Volkow N.D., Wang G.J., Fowler J.S., Logan J., Gatley S.J., Hitzemann R., Chen A.D., Dewey S.L., Pappas N. Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature 1997, 386:830-833.
63. Weiss F., Markou A., Lorang M.T., Koob G.F. Basal extracellular dopamine levels in the nucleus accumbens are decreased during cocaine withdrawal after unlimited-access self-administration. Brain Res 1992, 593:314-318.
64. Weiss F., Paulus M.P., Lorang M.T., Koob G.F. Increases in extracellular dopamine in the nucleus accumbens by cocaine are inversely related to basal levels: effects of acute and repeated administration. J Neurosci 1992, 12:4372-4380.
65. Wilson J.M., Levey A.I., Bergeron C., Kalasinsky K., Ang L., Peretti F., Adams V.I., Smialek J., Anderson W.R., Shannak K., Deck J., Niznik H.B., Kish S.J. Striatal dopamine, dopamine transporter, and vesicular monoamine transporter in chronic cocaine users. Ann Neurol 1996, 40:428-439.
66. Woolverton W.L. Effects of a D1 and a D2 dopamine antagonist on the self-administration of cocaine and piribedil by rhesus monkeys. Pharmacol Biochem Behav 1986, 24:531-535.
67. Wu J.C., Bell K., Najafi A., Widmark C., Keator D., Tang C., Klein E., Bunney B.G., Fallon J., Bunney W.E. Decreasing striatal 6-FDOPA uptake with increasing duration of cocaine withdrawal. Neuropsychopharmacology 1997, 17:402-409.