In vivo ethanol experience increases D 2 autoinhibition in the ventral tegmental area

Neuropsychopharmacology

Volumn 36, Issue 5, 2011, Pages 993-1002

  Perra, Simona ^a   Clements, Michael A ^a   Bernier, Brian E ^a   Morikawa, Hitoshi ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

alcoholism; calcium; D 2 receptor; desensitization; dopamine neuron; ethanol

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; ALCOHOL; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; DOPAMINE; DOPAMINE 2 RECEPTOR; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; METABOTROPIC RECEPTOR;

ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DESENSITIZATION; DOPAMINERGIC NERVE CELL; ELECTROPHYSIOLOGY; ENVIRONMENTAL EXPOSURE; MALE; MOUSE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VENTRAL TEGMENTUM;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BACLOFEN; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CHELATING AGENTS; DOPAMINE; DOPAMINE AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EGTAZIC ACID; ELECTRIC STIMULATION; ENZYME INHIBITORS; ESTRENES; ETHANOL; GABA ANTAGONISTS; GABA-B RECEPTOR AGONISTS; INDOLES; MALE; METHOXYHYDROXYPHENYLGLYCOL; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; NEURONS; ORGANOPHOSPHORUS COMPOUNDS; PATCH-CLAMP TECHNIQUES; PYRROLIDINONES; RECEPTORS, DOPAMINE D2; TIME FACTORS; VENTRAL TEGMENTAL AREA;

EID: 79952747317     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2010.237     Document Type: Article

References (70)

1. Ahn KC, Bernier BE, Harnett MT, Morikawa H (2010). IP3 receptor sensitization during in vivo amphetamine experience enhances NMDA receptor plasticity in dopamine neurons of the ventral tegmental area. J Neurosci 30: 6689-6699.
2. Backes E, Hemby SE (2003). Discrete cell gene profiling of ventral tegmental dopamine neurons after acute and chronic cocaine self-administration. J Pharmacol Exp Ther 307: 450-459. (Pubitemid 37310656)
3. Beckstead MJ, Gantz SC, Ford CP, Stenzel-Poore MP, Phillips PE, Mark GP et al (2009). CRF enhancement of GIRK channel-mediated transmission in dopamine neurons. Neurop-sychopharmacology 34: 1926-1935.
4. Beckstead MJ, Grandy DK, Wickman K, Williams JT (2004). Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons. Neuron 42: 939-946. (Pubitemid 38798232)
5. Beckstead MJ, Williams JT (2007). Long-term depression of a dopamine IPSC. J Neurosci 27: 2074-2080.
6. Boileau I, Assaad JM, Pihl RO, Benkelfat C, Leyton M, Diksic M et al (2003). Alcohol promotes dopamine release in the human nucleus accumbens. Synapse 49: 226-231. (Pubitemid 36927963)
7. Brodie MS (2002). Increased ethanol excitation of dopaminergic neurons of the ventral tegmental area after chronic ethanol treatment. Alcohol Clin Exp Res 26: 1024-1030. (Pubitemid 34778780)
8. Brodie MS, Shefner SA, Dunwiddie TV (1990). Ethanol increases the firing rate of dopamine neurons of the rat ventral tegmental area in vitro. Brain Res 508: 65-69. (Pubitemid 20042066)
9. Cruz HG, Ivanova T, Lunn ML, Stoffel M, Slesinger PA, Luscher C (2004). Bi-directional effects of GABA(B) receptor agonists on the mesolimbic dopamine system. Nat Neurosci 7: 153-159. (Pubitemid 38129791)
10. Cui G, Bernier BE, Harnett MT, Morikawa H (2007). Differential regulation of action potential- and metabotropic glutamate receptor-induced Ca2+ signals by inositol 1,4,5-trisphosphate in dopaminergic neurons. J Neurosci 27: 4776-4785. (Pubitemid 46663569)
11. Davila V, Yan Z, Craciun LC, Logothetis D, Sulzer D (2003). D3 dopamine autoreceptors do not activate G-protein-gated inwardly rectifying potassium channel currents in substantia nigra dopamine neurons. J Neurosci 23: 5693-5697. (Pubitemid 36807847)
12. Diana M, Pistis M, Carboni S, Gessa GL, Rossetti ZL (1993). Profound decrement of mesolimbic dopaminergic neuronal activity during ethanol withdrawal syndrome in rats: electrophysiological and biochemical evidence. Proc Natl Acad Sci USA 90: 7966-7969. (Pubitemid 23260835)
13. Diana M, Pistis M, Muntoni A, Gessa G (1996). Mesolimbic dopaminergic reduction outlasts ethanol withdrawal syndrome: evidence of protracted abstinence. Neuroscience 71: 411-415. (Pubitemid 26067011)
14. Diana M, Pistis M, Muntoni AL, Gessa GL (1995). Ethanol withdrawal does not induce a reduction in the number of spontaneously active dopaminergic neurons in the mesolimbic system. Brain Res 682: 29-34.
15. Erhardt S, Mathe JM, Chergui K, Engberg G, Svensson TH (2002). GABA(B) receptor-mediated modulation of the firing pattern of ventral tegmental area dopamine neurons in vivo. Naunyn Schmiedebergs Arch Pharmacol 365: 173-180. (Pubitemid 34212227)
16. Ford CP, Mark GP, Williams JT (2006). Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location. J Neurosci 26: 2788-2797. (Pubitemid 43357862)
17. Gallegos RA, Lee RS, Criado JR, Henriksen SJ, Steffensen SC (1999). Adaptive responses of gamma-aminobutyric acid neurons in the ventral tegmental area to chronic ethanol. J Pharmacol Exp Ther 291: 1045-1053.
18. George SR, Fan T, Ng GY, Jung SY, O'Dowd BF, Naranjo CA (1995). Low endogenous dopamine function in brain predisposes to high alcohol preference and consumption: reversal by increasing synaptic dopamine. J Pharmacol Exp Ther 273: 373-379.
19. Gessa GL, Muntoni F, Collu M, Vargiu L, Mereu G (1985). Low doses of ethanol activate dopaminergic neurons in the ventral tegmental area. Brain Res 348: 201-203. (Pubitemid 16235764)
20. Gordon AS, Yao L, Jiang Z, Fishburn CS, Fuchs S, Diamond I (2001). Ethanol acts synergistically with a D2 dopamine agonist to cause translocation of protein kinase C. Mol Pharmacol 59: 153-160. (Pubitemid 32043097)
21. Gu Z, Yan Z (2004). Bidirectional regulation of Ca2+/calmodulin-dependent protein kinase II activity by dopamine D4 receptors in prefrontal cortex. Mol Pharmacol 66: 948-955. (Pubitemid 39319467)
22. Henry DJ, Greene MA, White FJ (1989). Electrophysiological effects of cocaine in the mesoaccumbens dopamine system: repeated administration. J Pharmacol Exp Ther 251: 833-839. (Pubitemid 20024893)
23. Hernandez-Lopez S, Tkatch T, Perez-Garci E, Galarraga E, Bargas J, Hamm H et al (2000). D2 dopamine receptors in striatal medium spiny neurons reduce L-type Ca2+ currents and excitability via a novel PLC[beta]1-IP3-calcineurin- signaling cascade. J Neurosci 20: 8987-8995. (Pubitemid 32042899)
24. Hopf FW, Martin M, Chen BT, Bowers MS, Mohamedi MM, Bonci A (2007). Withdrawal from intermittent ethanol exposure increases probability of burst firing in VTA neurons in vitro. J Neurophysiol 98: 2297-2310. (Pubitemid 47584414)
25. Hu XT, Dong Y, Zhang XF, White FJ (2005). Dopamine D2 receptor-activated Ca2+ signaling modulates voltage-sensitive sodium currents in rat nucleus accumbens neurons. J Neuro-physiol 93: 1406-1417. (Pubitemid 40283729)
26. Ikemoto S (2007). Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56: 27-78. (Pubitemid 350110353)
27. 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. (Pubitemid 16006360)
28. Koob GF (2009). Neurobiological substrates for the dark side of compulsivity in addiction. Neuropharmacology 56(Suppl 1): 18-31.
29. Koob GF, Volkow ND (2010). Neurocircuitry of addiction. Neuropsychopharmacology 35: 217-238.
30. Labouebe G, Lomazzi M, Cruz HG, Creton C, Lujan R, Li M et al (2007). RGS2 modulates coupling between GABAB receptors and GIRK channels in dopamine neurons of the ventral tegmental area. Nat Neurosci 10: 1559-1568. (Pubitemid 350175875)
31. Lacey MG, Mercuri NB, North RA (1987). Dopamine acts on D2 receptors to increase potassium conductance in neurones of the rat substantia nigra zona compacta. J Physiol 392: 397-416. (Pubitemid 18014315)
32. Lammel S, Hetzel A, Hackel O, Jones I, Liss B, Roeper J (2008). Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 57: 760-773. (Pubitemid 351335346)
33. Licata SC, Schmidt HD, Pierce RC (2004). Suppressing calcium/calmodulin- dependent protein kinase II activity in the ventral tegmental area enhances the acute behavioural response to cocaine but attenuates the initiation of cocaine-induced behavioural sensitization in rats. Eur J Neurosci 19: 405-414. (Pubitemid 38177879)
34. Liu XY, Mao LM, Zhang GC, Papasian CJ, Fibuch EE, Lan HX et al (2009). Activity-dependent modulation of limbic dopamine D3 receptors by CaMKII. Neuron 61: 425-438.
35. Luscher C, Slesinger PA (2010). Emerging roles for G protein-gated inwardly rectifying potassium (GIRK) channels in health and disease. Nat Rev Neurosci 11: 301-315.
36. Margolis EB, Lock H, Hjelmstad GO, Fields HL (2006). The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? J Physiol 577(Part 3): 907-924. (Pubitemid 44873655)
37. Marinelli M, Cooper DC, Baker LK, White FJ (2003). Impulse activity of midbrain dopamine neurons modulates drug-seeking behavior. Psychopharmacology (Berl) 168: 84-98. (Pubitemid 36851166)
38. Martinez D, Gil R, Slifstein M, Hwang DR, Huang Y, Perez A et al (2005). Alcohol dependence is associated with blunted dopamine transmission in the ventral striatum. Biol Psychiatry 58: 779-786. (Pubitemid 41677416)
39. McBride WJ, Bodart B, Lumeng L, Li TK (1995). Association between low contents of dopamine and serotonin in the nucleus accumbens and high alcohol preference. Alcohol Clin Exp Res 19: 1420-1422. (Pubitemid 26005687)
40. Melis M, Camarini R, Ungless MA, Bonci A (2002). Long-lasting potentiation of GABAergic synapses in dopamine neurons after a single in vivo ethanol exposure. J Neurosci 22: 2074-2082. (Pubitemid 35386508)
41. Melis M, Spiga S, Diana M (2005). The dopamine hypothesis of drug addiction: hypodopaminergic state. Int Rev Neurobiol 63: 101-154. (Pubitemid 43631260)
42. Michler A, Erdo SL (1989). Stimulation by phaclofen of inositol 1,4,5-triphosphate production in cultured neurons from chick tectum. Eur J Pharmacol 167: 423-425. (Pubitemid 19216549)
43. Morikawa H, Morrisett RA (2010). Ethanol action on dopaminergic neurons in the ventral tegmental area: interaction with intrinsic ion channels and neurotransmitter inputs. Int Rev Neurobiol 91: 235-288.
44. Morris SJ, Van II H, Daigle M, Robillard L, Sajedi N, Albert PR (2007). Differential desensitization of dopamine D2 receptor iso-forms by protein kinase C: the importance of receptor phosphoryla-tion and pseudosubstrate sites. Eur J Pharmacol 577: 44-53. (Pubitemid 47632523)
45. Mutneja M, Berton F, Suen KF, Luscher C, Slesinger PA (2005). Endogenous RGS proteins enhance acute desensitization of GABA(B) receptor-activated GIRK currents in HEK-293T cells. Pflugers Arch 450: 61-73. (Pubitemid 40558533)
46. Namkung Y, Sibley DR (2004). Protein kinase C mediates phosphorylation, desensitization, and trafficking of the D2 dopamine receptor. J Biol Chem 279: 49533-49541. (Pubitemid 39625841)
47. Neuhoff H, Neu A, Liss B, Roeper J (2002). I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 22: 1290-1302. (Pubitemid 34163731)
48. Okamoto T, Harnett MT, Morikawa H (2006). Hyperpolarization-activated cation current (Ih) is an ethanol target in midbrain dopamine neurons of mice. J Neurophysiol 95: 619-626. (Pubitemid 44699069)
49. Parramon M, Gonzalez MP, Herrero MT, Oset-Gasque MJ (1995). GABAB receptors increase intracellular calcium concentrations in chromaffin cells through two different pathways: their role in catecholamine secretion. J Neurosci Res 41: 65-72.
50. Pucak ML, Grace AA (1994). Evidence that systemically administered dopamine antagonists activate dopamine neuron firing primarily by blockade of somatodendritic autoreceptors. J Pharmacol Exp Ther 271: 1181-1192. (Pubitemid 24382619)
51. Putzier I, Kullmann PH, Horn JP, Levitan ES (2009). Dopamine neuron responses depend exponentially on pacemaker interval. J Neurophysiol 101: 926-933.
52. Riegel AC, Williams JT (2008). CRF facilitates calcium release from intracellular stores in midbrain dopamine neurons. Neuron 57: 559-570. (Pubitemid 351273995)
53. Rossetti ZL, Melis F, Carboni S, Gessa GL (1992). Dramatic depletion of mesolimbic extracellular dopamine after withdrawal from morphine, alcohol or cocaine: a common neurochemical substrate for drug dependence. Ann NY Acad Sci 654: 513-516.
54. Seidler NW, Jona I, Vegh M, Martonosi A (1989). Cyclopiazonic acid is a specific inhibitor of the Ca2+-ATPase of sarcoplasmic reticulum. J Biol Chem 264: 17816-17823. (Pubitemid 19279247)
55. Shen RY (2003). Ethanol withdrawal reduces the number of spontaneously active ventral tegmental area dopamine neurons in conscious animals. J Pharmacol Exp Ther 307: 566-572.
56. Shen RY, Chiodo LA (1993). Acute withdrawal after repeated ethanol treatment reduces the number of spontaneously active dopaminergic neurons in the ventral tegmental area. Brain Res 622: 289-293. (Pubitemid 23264977)
57. Sinha R (2008). Chronic stress, drug use, and vulnerability to addiction. Ann NY Acad Sci 1141: 105-130.
58. Takeuchi Y, Fukunaga K, Miyamoto E (2002). Activation of nuclear Ca(2+)/calmodulin-dependent protein kinase II and brain-derived neurotrophic factor gene expression by stimulation of dopamine D2 receptor in transfected NG108-15 cells. J Neurochem 82: 316-328. (Pubitemid 34774622)
59. Trevisan LA, Boutros N, Petrakis IL, Krystal JH (1998). Complications of alcohol withdrawal: pathophysiological insights. Alcohol Health Res World 22: 61-66.
60. Ungless MA, Argilli E, Bonci A (2010). Effects of stress and aversion on dopamine neurons: implications for addiction. Neurosci Biobehav Rev 35: 151-156.
61. Vallar L, Muca C, Magni M, Albert P, Bunzow J, Meldolesi J et al (1990). Differential coupling of dopaminergic D2 receptors expressed in different cell types. Stimulation of phosphatidyli-nositol 4,5-bisphosphate hydrolysis in LtK- fibroblasts, hyper-polarization, and cytosolic-free Ca2+ concentration decrease in GH4C1 cells. J Biol Chem 265: 10320-10326.
62. Volkow ND, Wang GJ, Telang F, Fowler JS, Logan J, Jayne M et al (2007). Profound decreases in dopamine release in striatum in detoxified alcoholics: possible orbitofrontal involvement. J Neurosci 27: 12700-12706. (Pubitemid 350127825)
63. Wanat MJ, Hopf FW, Stuber GD, Phillips PE, Bonci A (2008). Corticotropin-releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C-dependent enhancement of Ih. J Physiol 586: 2157-2170. (Pubitemid 351524569)
64. Wee S, Koob GF (2010). The role of the dynorphin-kappa opioid system in the reinforcing effects of drugs of abuse. Psychophar-macology (Berl) 210: 121-135.
65. Weiss F, Lorang MT, Bloom FE, Koob GF (1993). Oral alcohol self-administration stimulates dopamine release in the rat nucleus accumbens: genetic and motivational determinants. J Pharmacol Exp Ther 267: 250-258. (Pubitemid 23325015)
66. Weiss F, Parsons LH, Schulteis G, Hyytia P, Lorang MT, Bloom FE et al (1996). Ethanol self-administration restores withdrawal-associated deficiencies in accumbal dopamine and 5-hydroxytryptamine release in dependent rats. J Neurosci 16: 3474-3485. (Pubitemid 26142376)
67. Werkman TR, Kruse CG, Nievelstein H, Long SK, Wadman WJ (2001). In vitro modulation of the firing rate of dopamine neurons in the rat substantia nigra pars compacta and the ventral tegmental area by antipsychotic drugs. Neuropharmacol-ogy 40: 927-936. (Pubitemid 32510806)
68. White FJ, Wang RY (1984). A10 dopamine neurons: role of autoreceptors in determining firing rate and sensitivity to dopamine agonists. Life Sci 34: 1161-1170. (Pubitemid 14161730)
69. Wolf ME, White FJ, Nassar R, Brooderson RJ, Khansa MR (1993). Differential development of autoreceptor subsensitivity and enhanced dopamine release during amphetamine sensitization. J Pharmacol Exp Ther 264: 249-255. (Pubitemid 23309209)
70. Zhang TA, Placzek AN, Dani JA (2010). In vitro identification and electrophysiological characterization of dopamine neurons in the ventral tegmental area. Neuropharmacology 59: 431-436.