Limited access to ethanol increases the number of spontaneously active dopamine neurons in the posterior ventral tegmental area of nondependent P rats

Alcohol

Volumn 44, Issue 3, 2010, Pages 257-264

  Morzorati, Sandra L ^a   Marunde, Rita L ^a   Downey, David ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alcohol preferring (P) rats; Chronic ethanol consumption; Dopamine neurons; Spontaneously active dopamine neurons; Ventral tegmental area

Indexed keywords

ALCOHOL; DOPAMINE;

ALCOHOL CONSUMPTION; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; FEMALE; FLUID INTAKE; IN VIVO STUDY; LIMBIC SYSTEM; NERVE CELL EXCITABILITY; NERVE ENDING; NONHUMAN; NUCLEUS ACCUMBENS; RAT; VENTRAL TEGMENTUM;

ACTION POTENTIALS; ALCOHOL DRINKING; ANIMALS; DOPAMINE; ETHANOL; FEMALE; NEURONS; RATS; RATS, INBRED STRAINS; VENTRAL TEGMENTAL AREA;

RATTUS;

EID: 77953512855     PISSN: 07418329     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.alcohol.2010.02.009     Document Type: Article

References (80)

1. Alheid G.F., De Olmos J.S., Beltramino C.A. Amygdala and extended amygdala. The Rat Nervous System 1995, 495-578. Academic Press, San Diego, CA. 2nd ed. G. Paxinos (Ed.).
2. Allan A.M., Harris R.A. Involvement of neuronal chloride channel in ethanol intoxication, tolerance, and dependence. Recent Dev. Alcohol. 1987, 5:313-325.
3. Appel S.B., Liu Z., Mcelvain A., Brodie M.S. Ethanol excitation of dopaminergic ventral tegmental area neurons is blocked by quinidine. J. Pharmacol. Exp. Ther. 2003, 306:437-446.
4. Brodie M.S. Increased ethanol excitation of dopaminergic neurons of the ventral tegmental area after chronic ethanol treatment. Alcohol. Clin. Exp. Res. 2002, 26:1024-1030.
5. Brodie M.S., Pesold C., Appel S.B. Ethanol directly excites dopaminergic ventral tegmental area reward neurons. Alcohol. Clin. Exp. Res. 1999, 23:1848-1852.
6. Brodie M.S., Shefner S.A., Dunwiddie T.V. Ethanol increases the firing rate of dopamine neurons of the rat ventral tegmental area in vitro. Brain Res. 1990, 508:65-69.
7. Bunney B.S., Aghajanian G.K., Roth R.H. Comparison of effects of L-dopa, amphetamine and apomorphine on firing rate of rat dopaminergic neurons. Nat. New Biol. 1973, 245:123-125.
8. Bunney B.S., Grace A.A. Acute and chronic haloperidol treatment: comparison of effects on nigral dopaminergic activity. Life Sci. 1978, 23:1715-1727.
9. Carpenter-Hyland E.P., Woodward J.J., Chandler L.J. Chronic ethanol induces synaptic but not extrasynaptic targeting of NMDA receptors. J. Neurosci. 2004, 24:7859-7868.
10. Chiodo L.A. Dopamine-containing neurons in the mammalian central nervous system: electrophysiology and pharmacology. Neurosci. Biobehav. Rev. 1988, 12:49-91.
11. Chiodo L.A., Bunney B.S. Typical and atypical neuroleptics; differential effects of chronic administration on the activity of A9 and A10 midbrain dopaminergic neurons. J. Neurosci. 1983, 3:1607-1619.
12. Chiodo L.A., Caggiula A.R. Substantia nigra dopamine neurons: alterations in basal discharge rates and autoreceptor sensitivity induced by estrogen. Neuropharmacology 1983, 22:593-599.
13. Christie M.J., Bridge S., James L.B., Beart P.M. Excitotoxic lesions suggest an aspartatergic projection from the medial prefrontal cortex to the ventral tegmental area. Brain Res. 1985, 333:169-172.
14. Cicero T.J. Animal models of alcoholism. Animal Models in Alcohol Research 1980, 99-117. Academic Press, New York, NY. K. Eriksson, J.D. Sinclair, K. Kiianmaa (Eds.).
15. Clement J.R., Grant S. Glutamate-like immunoreactivity in neurons of the rat laterodorsal and pedunculopontine nucleus in the rat. Neurosci. Lett. 1990, 120:70-73.
16. Creutz L.M., Kritzer M.F. Estrogen receptor-β immunoreactivity in the midbrain of adult rats: regional, subregional, and cellular localization in the A10, A9, and A8 dopamine cell groups. J. Comp. Neurol. 2002, 446:288-300.
17. 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.
18. Diana M., Pistis M., Muntoni A., Gessa G. Mesolimbic dopaminergic reduction outlasts ethanol withdrawal syndrome: evidence of protracted abstinence. Neuroscience 1996, 71:411-415.
19. DiChiara G., Imperato A. Ethanol preferentially stimulates dopamine release in the nucleus accumbens of freely moving rats. Eur. J. Pharmacol. 1985, 115:131-132.
20. Engleman E.A., McBride W.J., Li T.-K., Lumeng L., Murphy J.M. Ethanol drinking experience attenuates (-)sulpiride-induced increases in extracellular dopamine levels in the nucleus accumbens of alcohol-preferring (P) rats. Alcohol. Clin. Exp. Res. 2003, 27:424-431.
21. Engleman E.A., McBride W.J., Wilber A.A., Shaikh S.R., Eha R.D., Lumeng L., et al. Reverse microdialysis of a dopamine uptake inhibitor in the nucleus accumbens of alcohol-preferring rats; effects on dialysate dopamine levels and ethanol intake. Alcohol. Clin. Exp. Res. 2000, 24:795-801.
22. Floresco S.B., West A.R., Ash B., Moore H., Grace A.A. Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat. Neurosci. 2003, 6:968-973.
23. Follesa P., Ticku M.K. Chronic ethanol treatment differentially regulates NMDA receptor subunit mRNA expression in rat brain. Mol. Brain Res. 1995, 29:99-106.
24. Freeman A.S., Bunney B.S. Activity of A9 and A10 dopaminergic neurons in unrestrained rats: further characterization and effects of apomorphine and cholecystokinin. Brain Res. 1987, 405:46-55.
25. Gariano R.F., Groves P.M. Burst firing induced in midbrain dopamine neurons by stimulation of the medial prefrontal and anterior cingulate cortices. Brain Res. 1988, 462:194-198.
26. Gatto G.J., McBride W.J., Murphy J.M., Lumeng L., Li T.-K. Ethanol self-infusion into the ventral tegmental area by alcohol-preferring rats. Alcohol 1994, 11:557-564.
27. Gessa G.L., Muntoni F., Collu M., Vargiu L., Mereu G. Low doses of ethanol activate dopaminergic neurons in the ventral tegmental area. Brain Res. 1985, 348:201-203.
28. Gonon F. Nonlinear relationship between impulse flow and dopamine released by rat midbrain neurons as studied by in vivo electrochemistry. Neuroscience 1988, 24:19-28.
29. Grace A.A. The regulation of dopamine neuron activity as determined by in vivo and in vitro intracellular recordings. Neurophysiology of Dopaminergic Systems-Current Status and Clinical Perspectives 1987, 1-66. Lakeshore Publishing, Detroit, MI. L.A. Chiodo, A.S. Freeman (Eds.).
30. Grace A.A. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 1991, 41:1-24.
31. Grace A.A., Bunney B.S. Intracellular and extracellular electrophysiology of nigral dopaminergic neurons. I. Identification and characterization. Neuroscience 1983, 10:301-315.
32. Grace A.A., Bunney B.S. The control of firing pattern in nigral dopamine neurons: burst firing. J. Neurosci. 1984, 4:2877-2890.
33. Groves P.M., Wilson C.J., Young S.J., Rebec G.V. Self-inhibition by dopaminergic neurons. Science 1975, 190:522-529.
34. Holter S.M., Danysz W., Spanagel R. Novel uncompetitive N-methyl-D-aspartate (NMDA)-receptor antagonist MRZ 2/579 suppresses ethanol intake in long-term ethanol-experienced rats and generalizes to ethanol cue in drug discrimination procedure. J. Pharmacol. Exp. Ther. 2000, 292:545-552.
35. Ikemoto S. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Rev. 2007, 56:27-78.
36. Ikemoto S., Qin M., Liu Z.H. Primary reinforcing effects of nicotine are triggered from multiple regions both inside and outside the ventral tegmental area. J. Neurosci. 2006, 26:723-730.
37. Ikemoto S., Wise R.A. Rewarding effects of the cholinergic agents carbachol and neostigmine in the posterior ventral area. J. Neurosci. 2002, 22:9895-9904.
38. Imperato A., DiChiara G. Preferential stimulation of dopamine release in the nucleus accumbens of freely moving rats by ethanol. J. Pharmacol. Exp. Ther. 1986, 239:219-228.
39. Johnson S.W., North R.A. Two types of neurons in the rat ventral tegmental area and their synaptic inputs. J. Physiol. (Lond) 1992, 450:455-468.
40. Kang M.H., Spigelman I., Olsen R.W. Alteration in the sensitivity of GABA(A) receptors to allosteric modulatory drugs in rat hippocampus after chronic intermittent ethanol treatment. Alcohol. Clin. Exp. Res. 1998, 22:2165-2173.
41. Kang M.H., Spigelman I., Sapp D.D., Olsen R.W. Persistent reduction of GABA(A) receptor-mediated inhibition in rat hippocampus after chronic intermittent ethanol treatment. Brain Res. 1996, 709:221-228.
42. Kelland M.D., Chiodo L.A., Freeman A.S. Anesthetic influences on the basal activity and pharmacological responsiveness of nigrostriatal dopamine neurons. Synapse 1990, 3:207-209.
43. Kelland M.D., Freeman A.S., Chiodo L.A. Chloral hydrate anesthesia alters the responsiveness of identified midbrain dopamine neurons to dopamine agonist administration. Synapse 1989, 3:30-37.
44. Kitai S.T., Shepard P.D., Callaway J.C., Scroggs R. Afferent modulation of dopamine neuron firing patterns. Curr. Opin. Neurobiol. 1999, 9:690-697.
45. Koob G.F., Bloom F.E. Cellular and molecular mechanisms of drug dependence. Science 1988, 242:715-723.
46. Koob G.F., Weiss F. Neuropharmacology of cocaine and ethanol dependence. Recent Dev. Alcohol. 1992, 10:201-233.
47. A receptors: genomic and nongenomic mechanisms. Pharmacol. Ther. 2004, 101:211-226.
48. Kumari M., Ticku M.K. Regulation of NMDA receptors by ethanol. Prog. Drug Res. 2000, 54:152-189.
49. Lumeng L., Hawkins D.T., Li T.-K. New strains of rats with alcohol preference and nonpreference. Alcohol and Metabolizing Systems 1977, Vol. 3:537-544. Academic Press, New York, NY. R.G. Thurman, J.R. Williamson, H. Drott, B. Chance (Eds.).
50. Melendez R.I., Rodd-Hendricks Z.A., Engleman E.A., Li T.-K., McBride W.J., Murphy J.M. Microdialysis of dopamine in the nucleus accumbens of alcohol preferring (P) rats during anticipation and operant self-administration of ethanol. Alcohol. Clin. Exp. Res. 2002, 26:318-325.
51. Moore H., Todd C.L., Grace A.A. Striatal extracellular dopamine levels in rats with haloperidol-induced depolarization block of substantia nigra dopamine neurons. J. Neurosci. 1998, 18:5068-5077.
52. Morzorati S.L., Marunde R.L. Comparison of VTA dopamine neuron activity in lines of rats selectively bred to prefer or avoid alcohol. Alcohol. Clin. Exp. Res. 2006, 30:991-997.
53. Murphy J.M., Gatto G.J., McBride W.J., Lumeng L., Li T.-K. Operant responding for oral ethanol in the alcohol-preferring P and alcohol-nonpreferring NP lines of rats. Alcohol 1989, 6:127-131.
54. Murphy J.M., Gatto G.J., Waller M.B., McBride W.J., Lumeng L., Li T.-K. Effects of scheduled access on ethanol intake by the alcohol-preferring (P) line of rats. Alcohol 1986, 3:331-336.
55. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, New York, NY. 4th ed.
56. Rodd Z.A., Bell R.L., Kuc K.A., Zhang Y., Murphy J.M., McBride J.M. Intracranial self-administration of cocaine within the posterior ventral tegmental area of Wistar rats: evidence for involvement of serotonin-3 receptors and dopamine neurons. J. Pharmacol. Exp. Ther. 2005, 313:134-145.
57. Rodd Z.A., Bell R.L., Zhang Y., Murphy J.M., Goldstein A., Zaffaroni A., et al. Regional heterogeneity for intracranial self-administration of ethanol and acetaldehyde within the ventral tegmental area of alcohol-preferring (P) rats: involvement of dopamine and serotonin. Neuropsychopharmacology 2005, 30:330-338.
58. Rodd Z.A., Melendez R.I., Bell R.L., Kuc K.A., Zhang Y., Murphy J.M., et al. Intracranial self-administration of ethanol within the ventral tegmental area of male Wistar rats: evidence for regional heterogeneity and involvement of dopamine neurons. J. Neurosci. 2004, 24:1050-1057.
59. Rodd-Hendricks Z.A., McKinzie D.L., Crile R.S., Murphy J.M., McBride W.J. Regional heterogeneity for the intracranial self-administration of ethanol within the ventral tegmental area of female Wistar rats. Psychopharmacology 2000, 149:217-224.
60. Rodd-Hendricks Z.A., Melendez R.I., Zaffaroni A., Goldstein A., McBride W.J., Li T.-K. The reinforcing effects of acetaldehyde in the posterior ventral tegmental area of alcohol-preferring rats. Pharmacol. Biochem. Behav. 2002, 72:55-64.
61. Shen R.-Y. Ethanol withdrawal reduces the number of spontaneously active VTA dopamine neurons in conscious animals. J. Pharmacol. Exp. Ther. 2003, 307:566-572.
62. Shen R.-Y., Chiodo L.A. Acute withdrawal after repeated ethanol treatment reduces the number of spontaneously active dopaminergic neurons in the ventral tegmental area. Brain Res. 1993, 622:289-293.
63. Shen R.-Y., Choong K.-C., Thompson A.C. Long-term reduction in ventral tegmental area dopamine neuron population activity following repeated stimulant or ethanol treatment. Biol. Psychiatry 2007, 61:93-100.
64. Smith A.D., Weiss F. Ethanol exposure differentially alters central monoamine neurotransmission in alcohol-preferring versus -nonpreferring rats. J. Pharmacol. Exp. Ther. 1999, 288:1223-1228.
65. Starke K., Gothert M., Kilbinger H. Modulation of neurotransmitter release by presynaptic autoreceptors. Physiol. Rev. 1989, 69:864-989.
66. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 1982, 9:321-353.
67. Tepper J.M., Gariano R.F., Groves P.M. The neurophysiology of dopamine nerve terminal autoreceptors. Neurophysiology of Dopaminergic Systems: Current Status and Clinical Perspectives 1987, 93-127. Lakeshore Publishing, Detroit, MI. L.A. Chiodo, A.S. Freeman (Eds.).
68. Thielen R.J., Engleman E.A., Rodd Z.A., Murphy J.M., Lumeng L., Li T.-K., et al. Ethanol drinking and deprivation alter dopaminergic and serotonergic function in the nucleus accumbens of alcohol-preferring rats. J. Pharmacol. Exp. Ther. 2004, 309:216-225.
69. Thompson T.L., Moss R.L. Estrogen regulation of dopamine release in the nucleus accumbens: genomic- and nongenomic-mediated effects. J. Neurochem. 1994, 62:1750-1756.
70. Tsai G., Colye J.T. The role of glutaminergic neurotransmission in the pathophysiology of alcoholism. Annu. Rev. Med. 1998, 49:173-184.
71. Waller M.B., McBride W.J., Lumeng L., Li T.-K. Induction of dependence on ethanol by free-choice drinking in alcohol preferring rats. Pharmacol. Biochem. Behav. 1982, 16:501-507.
72. Weiss F., Lorang M.T., Bloom F.E., Koob G.F. Oral alcohol self-administration stimulates dopamine release in the rat nucleus accumbens: genetic and motivational determinants. J. Pharmacol. Exp. Ther. 1993, 267:250-258.
73. Weiss F., Parsons L.H., Schulteis G., Hyytia P., Lorang M.T., Bloom F.E., et al. Ethanol self-administration restores withdrawal-associated deficiencies in accumbal dopamine and 5-hydroxytryptamine release in dependent rats. J. Neurosci. 1996, 16:3473-3485.
74. White F.J., Wang R.Y. Comparison of the effects of chronic haloperidol treatment on A9 and A10 dopamine neurons in the rat. Life Sci. 1983, 32:983-993.
75. Windels F., Kiyatkin E.A. General anesthesia as a factor affecting impulse activity and neuronal responses to putative neurotransmitters. Brain Res. 2006, 1086:104-116.
76. Wise R.A. The role of reward pathways in the development of drug dependence. Pharmacol. Ther. 1987, 35:227-263.
77. Wolf M.E., Roth R.H. Autoreceptor regulation of dopamine synthesis. Ann. N.Y. Acad. Sci. 1990, 604:323-343.
78. Yoshimoto K., McBride W.J., Lumeng L., Li T.-K. Alcohol stimulates the release of dopamine and serotonin in the nucleus accumbens. Alcohol 1991, 9:17-22.
79. Zangen A., Ikemoto S., Zadina J.E., Wise R.A. Rewarding and psychomotor stimulant effects of endomorphin-1: anteroposterior differences within the ventral tegmental area and lack of effect in nucleus accumbens. J. Neurosci. 2002, 22:7225-7233.
80. Zangen A., Solinas M., Ikemoto S., Goldberg S.R., Wise R.A. Two brain sites for cannabinoid reward. J. Neurosci. 2006, 26:4901-4907.