Ethanol- and cocaine-induced locomotion are genetically related to increases in accumbal dopamine

Genes, Brain and Behavior

Volumn 8, Issue 3, 2009, Pages 346-355

  Meyer, Paul J ^a   Meshul, Charles K ^a   Phillips, Tamara J ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b PORTLAND VA MEDICAL CENTER   (United States)

Author keywords

Alcohol abuse; Alcoholism; Behavioral genetics; Catecholamine; Cocaine; Excitatory amino acid; Motor behavior; Mouse; Psychostimulant; Selective breeding

Indexed keywords

ALCOHOL; COCAINE; DOPAMINE; GLUTAMIC ACID;

ALCOHOL ABUSE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CHEMOSENSITIVITY; DOPAMINERGIC NERVE CELL; DRUG EFFECT; GENETIC ASSOCIATION; GENETIC CORRELATION; LIMBIC CORTEX; LOCOMOTION; MICRODIALYSIS; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; STIMULUS RESPONSE;

ALCOHOL-INDUCED DISORDERS, NERVOUS SYSTEM; ANIMALS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; COCAINE; COCAINE-RELATED DISORDERS; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; ETHANOL; EXTRACELLULAR FLUID; GENETIC PREDISPOSITION TO DISEASE; MALE; MICE; MICE, MUTANT STRAINS; MICRODIALYSIS; MOTOR ACTIVITY; NEURAL PATHWAYS; NUCLEUS ACCUMBENS; SUBSTANCE-RELATED DISORDERS; VENTRAL TEGMENTAL AREA;

MUS;

EID: 63849116024     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2009.00481.x     Document Type: Article

References (70)

1. Addicott, M.A., Marsh-Richard, D.M., Mathias, C.W. Dougherty, D.M 2007) The biphasic effects of alcohol: comparisons of subjective and objective measures of stimulation, sedation, and physical activity. Alcohol Clin Exp Res 31, 1883 1890.
2. Amalric, M. Koob, G.F 1993) Functionally selective neurochemical afferents and efferents of the mesocorticolimbic and nigrostriatal dopamine system. Prog Brain Res 99, 209 226.
3. Beckstead M.J. Phillips, T.J 2009) Mice selectively bred for high or low alcohol-induced locomotion exhibit differences in dopamine neuron function. J Pharmacol Exp Ther epub ahead of print, January 2).
4. Bergstrom, H.C., Palmer, A.A., Wood, R.D., Burkhart-Kasch, S., McKinnon, C.S. Phillips, T.J 2003) Reverse selection for differential response to the locomotor stimulant effects of ethanol provides evidence for pleiotropic genetic influence on locomotor response to other drugs of abuse. Alcohol Clin Exp Res 27, 1535 1547.
5. Blednov, Y.A., Walker, D., Martinez, M., Levine, M., Damak, S. Margolskee, R.F 2008) Perception of sweet taste is important for voluntary alcohol consumption in mice. Genes Brain Behav 7, 1 13.
6. Blizard, D.A. McClearn, G.E 2000) Association between ethanol and sucrose intake in the laboratory mouse: exploration via congenic strains and conditioned taste aversion. Alcohol Clin Exp Res 24, 253 258.
7. Boehm, S.L. 2nd., Piercy, M.M., Bergstrom, H.C. Phillips, T.J 2002) Ventral tegmental area region governs GABA(B) receptor modulation of ethanol-stimulated activity in mice. Neuroscience 115, 185 200.
8. Budygin, E.A 2007) Dopamine uptake inhibition is positively correlated with cocaine-induced stereotyped behavior. Neurosci Lett 429, 55 58.
9. Chefer, V.I., Zakharova, I. Shippenberg, T.S 2003) Enhanced responsiveness to novelty and cocaine is associated with decreased basal dopamine uptake and release in the nucleus accumbens: quantitative microdialysis in rats under transient conditions. J Neurosci 23, 3076 3084.
10. Cosford, R.J., Parsons, L.H. Justice, J.B. Jr. 1994) Effect of tetrodotoxin and potassium infusion on microdialysis extraction fraction and extracellular dopamine in the nucleus accumbens. Neurosci Lett 178, 175 178.
11. Crabbe, J.C., Young, E.R., Deutsch, C.M., Tam, B.R. Kosobud, A 1987) Mice genetically selected for differences in open-field activity after ethanol. Pharmacol Biochem Behav 27, 577 581.
12. Dahchour, A., Hoffman, A., Deitrich, R. de Witte, P 2000) Effects of ethanol on extracellular amino acid levels in high-and low-alcohol sensitive rats: a microdialysis study. Alcohol Alcohol 35, 548 553.
13. Dahchour, A., Quertemont, E. De Witte, P 1994) Acute ethanol increases taurine but neither glutamate nor GABA in the nucleus accumbens of male rats: a microdialysis study. Alcohol Alcohol 29, 485 487.
14. Demarest, K., Hitzemann, B., Phillips, T. Hitzemann, R 1999) Ethanol-induced expression of c-Fos differentiates the FAST and SLOW selected lines of mice. Alcohol Clin Exp Res 23, 87 95.
15. Di Chiara, G. Imperato, A 1986) Preferential stimulation of dopamine release in the nucleus accumbens by opiates, alcohol, and barbiturates: studies with transcerebral dialysis in freely moving rats. Ann N Y Acad Sci 473, 367 381.
16. Downing, C., Carosone-Link, P., Bennett, B. Johnson, T 2006) QTL mapping for low-dose ethanol activation in the LXS recombinant inbred strains. Alcohol Clin Exp Res 30, 1111 1120.
17. Green, A.S. Grahame, N.J 2008) Ethanol drinking in rodents: is free-choice drinking related to the reinforcing effects of ethanol? Alcohol 42, 1 11.
18. Heinz, A., Schafer, M., Higley, J.D., Krystal, J.H. Goldman, D 2003) Neurobiological correlates of the disposition and maintenance of alcoholism. Pharmacopsychiatry 36 (Suppl. 3 S255 S258.
19. Holstein, S.E., Pastor, R., Meyer, P.J. Phillips, T.J 2005) Naloxone does not attenuate the locomotor effects of ethanol in FAST, SLOW, or two heterogeneous stocks of mice. Psychopharmacology (Berl) 182, 277 289.
20. Ikemoto, S. Panksepp, J 1999) The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev 31, 6 41.
21. Imperato, A. Di Chiara, G 1986) Preferential stimulation of dopamine release in the nucleus accumbens of freely moving rats by ethanol. J Pharmacol Exp Ther 239, 219 228.
22. Jerlhag, E 2008) The antipsychotic aripiprazole antagonizes the ethanol- and amphetamine-induced locomotor stimulation in mice. Alcohol 42, 123 127.
23. Kamens, H.M., Burkhart-Kasch, S., McKinnon, C.S., Li, N., Reed, C. Phillips, T.J 2006) Ethanol-related traits in mice selectively bred for differential sensitivity to methamphetamine-induced activation. Behav Neurosci 120, 1356 1366.
24. Kamens, H.M., McKinnon, C.S., Li, N., Helms, M.L., Belknap, J.K. Phillips, T.J 2009) The α3 subunit of the nicotinic acetylcholine receptor is a candidate gene for ethanol stimulation. Genes Brain Behav (epub ahead of print, September 30).
25. Kamens, H.M. Phillips, T.J 2008) A role for neuronal nicotinic acetylcholine receptors in ethanol-induced stimulation, but not cocaine- or methamphetamine-induced stimulation. Psychopharmacology 196, 377 387.
26. Kankaanpaa, A., Meririnne, E., Ariniemi, K. Seppala, T 2001) Oxalic acid stabilizes dopamine, serotonin, and their metabolites in automated liquid chromatography with electrochemical detection. J Chromatogr B Biomed Sci Appl 753, 413 419.
27. Kapasova, Z. Szumlinski, K.K 2008) Strain differences in alcohol-induced neurochemical plasticity: a role for accumbens glutamate in alcohol intake. Alcohol Clin Exp Res 32, 617 631.
28. King, A.C., Houle, T., de Wit, H., Holdstock, L. Schuster, A 2002) Biphasic alcohol response differs in heavy versus light drinkers. Alcohol Clin Exp Res 26, 827 835.
29. Kulkosky, P.J., Clayborne, Y.J. Sandoval, S.L 1993) Cholecystokinin and bombesin inhibit ethanol and food intake in rats selectively bred for ethanol sensitivity. Alcohol Clin Exp Res 17, 545 551.
30. LaLumiere, R.T. Kalivas, P.W 2008) Glutamate release in the nucleus accumbens core is necessary for heroin seeking. J Neurosci 28, 3170 3177.
31. Lominac, K.D., Kapasova, Z., Hannun, R.A., Patterson, C., Middaugh, L.D. Szumlinski, K.K 2006) Behavioral and neurochemical interactions between group 1 mGluR antagonists and ethanol: potential insight into their anti-addictive properties. Drug Alcohol Depend 85, 142 156.
32. Lovinger, D.M., White, G. Weight, F.F 1989) Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 243, 1721 1724.
33. McKee, B.L. Meshul, C.K 2005) Time-dependent changes in extracellular glutamate in the rat dorsolateral striatum following a single cocaine injection. Neuroscience 133, 605 613.
34. Meshul, C.K., Emre, N., Nakamura, C.M., Allen, C., Donohue, M.K. Buckman, J.F 1999) Time-dependent changes in striatal glutamate synapses following a 6-hydroxydopamine lesion. Neuroscience 88, 1 16.
35. Meyer, P.J. Phillips, T.J 2003) Sensitivity to ketamine, alone or in combination with ethanol, is altered in mice selectively bred for sensitivity to ethanol's locomotor effects. Alcohol Clin Exp Res 27, 1701 1709.
36. Mogenson, G.J. Yang, C.R 1991) The contribution of basal forebrain to limbic-motor integration and the mediation of motivation to action. Adv Exp Med Biol 295, 267 290.
37. Moghaddam, B. Bolinao, M.L 1994) Biphasic effect of ethanol on extracellular accumulation of glutamate in the hippocampus and the nucleus accumbens. Neurosci Lett 178, 99 102.
38. Moore, T.O., June, H.L. Lewis, M.J 1993) Ethanol-induced stimulation and depression on measures of locomotor activity: effects of basal activity levels in rats. Alcohol 10, 537 540.
39. Olive, M.F., Mehmert, K.K. Hodge, C.W 2000) Microdialysis in the mouse nucleus accumbens: a method for detection of monoamine and amino acid neurotransmitters with simultaneous assessment of locomotor activity. Brain Res Brain Res Protoc 5, 16 24.
40. Orsini, C., Buchini, F., Piazza, P.V., Puglisi-Allegra, S. Cabib, S 2004) Susceptibility to amphetamine-induced place preference is predicted by locomotor response to novelty and amphetamine in the mouse. Psychopharmacology (Berl) 172, 264 270.
41. Palmer, A.A., McKinnon, C.S., Bergstrom, H.C. Phillips, T.J 2002a) Locomotor activity responses to ethanol, other alcohols, and GABA-A acting compounds in forward- and reverse-selected FAST and SLOW mouse lines. Behav Neurosci 116, 958 967.
42. Palmer, A.A., Miller, M.N., McKinnon, C.S. Phillips, T.J 2002b) Sensitivity to the locomotor stimulant effects of ethanol and allopregnanolone is influenced by common genes. Behav Neurosci 116, 126 137.
43. Paxinos, G. Franklin, K.B 2001) The Mouse Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, San Diego, CA.
44. Pennartz, C.M., Groenewegen, H.J. Lopes da Silva, F.H 1994) The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog Neurobiol 42, 719 761.
45. Phillips, A.G., Blaha, C.D. Fibiger, H.C 1989) Neurochemical correlates of brain-stimulation reward measured by ex vivo and in vivo analyses. Neurosci Biobehav Rev 13, 99 104.
46. Phillips, T.J. Shen, E.H 1996) Neurochemical bases of locomotion and ethanol stimulant effects. Int Rev Neurobiol 39, 243 282.
47. Phillips, T.J., Burkhart-Kasch, S., Terdal, E.S. Crabbe, J.C 1991) Response to selection for ethanol-induced locomotor activation: genetic analyses and selection response characterization. Psychopharmacology (Berl) 103, 557 566.
48. Phillips, T.J., Burkhart-Kasch, S., Gwiazdon, C.C. Crabbe, J.C 1992) Acute sensitivity of FAST and SLOW mice to the effects of abused drugs on locomotor activity. J Pharmacol Exp Ther 261, 525 533.
49. Phillips, T.J., Shen, E.H., McKinnon, C.S., Burkhart-Kasch, S., Lessov, C.N. Palmer, A.A 2002) Forward, relaxed, and reverse selection for reduced and enhanced sensitivity to ethanol's locomotor stimulant effects in mice. Alcohol Clin Exp Res 26, 593 602.
50. Piepponen, T.P., Kiianmaa, K. Ahtee, L 2002) Effects of ethanol on the accumbal output of dopamine, GABA and glutamate in alcohol-tolerant and alcohol-nontolerant rats. Pharmacol Biochem Behav 74, 21 30.
51. Pierce, R.C., Bell, K., Duffy, P. Kalivas, P.W 1996) Repeated cocaine augments excitatory amino acid transmission in the nucleus accumbens only in rats having developed behavioral sensitization. J Neurosci 16, 1550 1560.
52. Ramachandra, V., Phuc, S., Franco, A.C. Gonzales, R.A 2007) Ethanol preference is inversely correlated with ethanol-induced dopamine release in 2 substrains of C57BL/6 mice. Alcohol Clin Exp Res 31, 1669 1676.
53. Ripley, T.L., Jaworski, J., Randall, P.K. Gonzales, R.A 1997) Repeated perfusion with elevated potassium in in vivo microdialysis - a method for detecting small changes in extracellular dopamine. J Neurosci Methods 78, 7 14.
54. Risinger, F.O., Malott, D.H., Prather, L.K., Niehus, D.R. Cunningham, C.L 1994) Motivational properties of ethanol in mice selectively bred for ethanol-induced locomotor differences. Psychopharmacology (Berl) 116, 207 216.
55. Rodd-Henricks, Z.A., McKinzie, D.L., Crile, R.S., Murphy, J.M. McBride, W.J 2000) Regional heterogeneity for the intracranial self-administration of ethanol within the ventral tegmental area of female Wistar rats. Psychopharmacology (Berl) 149, 217 224.
56. Schuckit, M.A 1994) Low level of response to alcohol as a predictor of future alcoholism. Am J Psychiatry 151, 184 189.
57. Schuckit, M.A., Smith, T.L., Trim, R., Kreikebaum, S., Hinga, B. Allen, R 2008) Testing the level of response to alcohol-based model of heavy drinking and alcohol problems in offspring from the San Diego Prospective Study. J Stud Alcohol Drugs 69, 571 579.
58. Selim, M. Bradberry, C.W 1996) Effect of ethanol on extracellular 5-HT and glutamate in the nucleus accumbens and prefrontal cortex: comparison between the Lewis and Fischer 344 rat strains. Brain Res 716, 157 164.
59. Shen, E.H., Harland, R.D., Crabbe, J.C. Phillips, T.J 1995) Bidirectional selective breeding for ethanol effects on locomotor activity: characterization of FAST and SLOW mice through selection generation 35. Alcohol Clin Exp Res 19, 1234 1245.
60. Shen, E.H., Dorow, J., Harland, R., Burkhart-Kasch, S. Phillips, T.J 1998) Seizure sensitivity and GABAergic modulation of ethanol sensitivity in selectively bred FAST and SLOW mouse lines. J Pharmacol Exp Ther 287, 606 615.
61. Smith, J.A., Mo, Q., Guo, H., Kunko, P.M. Robinson, S.E 1995) Cocaine increases extraneuronal levels of aspartate and glutamate in the nucleus accumbens. Brain Res 683, 264 269.
62. Szumlinski, K.K., Diab, M.E., Friedman, R., Henze, L.M., Lominac, K.D. Bowers, M.S 2007) Accumbens neurochemical adaptations produced by binge-like alcohol consumption. Psychopharmacology (Berl) 190, 415 431.
63. Thomas, D.N. Holman, R.B 1989) The effects of pH on amphetamine-induced dopamine release as measured by in vivo dialysis. Life Sci 45, 1299 1305.
64. Tzschentke, T.M. Schmidt, W.J 2000) Functional relationship among medial prefrontal cortex, nucleus accumbens, and ventral tegmental area in locomotion and reward. Crit Rev Neurobiol 14, 131 142.
65. Vengeliene, V., Bilbao, A., Molander, A. Spanagel, R 2008) Neuropharmacology of alcohol addiction. Br J Pharmacol 154, 299 315.
66. Waller, M.B., Murphy, J.M., McBride, W.J., Lumeng, L. Li, T.K 1986) Effect of low dose ethanol on spontaneous motor activity in alcohol-preferring and -nonpreferring lines of rats. Pharmacol Biochem Behav 24, 617 623.
67. Xu, Y., Demarest, K., Hitzemann, R. Sikela, J.M 2002) Gene coding variant in Cas1 between the C57BL/6J and DBA/2J inbred mouse strains: linkage to a QTL for ethanol-induced locomotor activation. Alcohol Clin Exp Res 26, 1 7.
68. Yim, H.J. Gonzales, R.A 2000) Ethanol-induced increases in dopamine extracellular concentration in rat nucleus accumbens are accounted for by increased release and not uptake inhibition. Alcohol 22, 107 115.
69. Zapata, A., Gonzales, R.A. Shippenberg, T.S 2006) Repeated ethanol intoxication induces behavioral sensitization in the absence of a sensitized accumbens dopamine response in C57BL/6J and DBA/2J mice. Neuropsychopharmacology 31, 396 405.
70. Zhang, Y., Loonam, T.M., Noailles, P.A. Angulo, J.A 2001) Comparison of cocaine- and methamphetamine-evoked dopamine and glutamate overflow in somatodendritic and terminal field regions of the rat brain during acute, chronic, and early withdrawal conditions. Ann N Y Acad Sci 937, 93 120.