Dual synaptic sites of D1-dopaminergic regulation of ethanol sensitivity of NMDA receptors in nucleus accumbens

Synapse

Volumn 58, Issue 1, 2005, Pages 30-44

  Zhang, Tao A ^a   Hendricson, Adam W ^a   Morrisett, Richard A ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Addiction; DARPP 32; Dependence; Mesolimbic; Reinforcement

Indexed keywords

2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; 8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; ALCOHOL; CALCIUM; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOPAMINE 1 RECEPTOR; DOPAMINE 1 RECEPTOR BLOCKING AGENT; DOPAMINE 1 RECEPTOR STIMULATING AGENT; MAGNESIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR SER987 NR1 SUBUNIT; PHOSPHOPROTEIN DARPP 32; RECEPTOR SUBUNIT; STRONTIUM; UNCLASSIFIED DRUG;

ADAPTATION; ADDICTION; ADOLESCENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CHEMOSENSITIVITY; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; DOSE RESPONSE; DRUG DEPENDENCE; ELECTROPHYSIOLOGY; FACILITATION; FEMALE; LIMBIC CORTEX; MALE; MEDIUM SPINY NERVE CELL; MINIATURE ENDPLATE POTENTIAL; NEUROMODULATION; NONHUMAN; NUCLEUS ACCUMBENS; PAIRED PULSE FACILITATION; POSTSYNAPTIC INHIBITION; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REINFORCEMENT; REWARD; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

2,3,4,5-TETRAHYDRO-7,8-DIHYDROXY-1-PHENYL-1H-3-BENZAZEPINE; ANIMALS; ANIMALS, NEWBORN; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DOPAMINE AGONISTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ELECTRIC STIMULATION; ETHANOL; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GABA ANTAGONISTS; MAGNESIUM; MALE; NEURONS; NUCLEUS ACCUMBENS; PATCH-CLAMP TECHNIQUES; PICROTOXIN; QUINOXALINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D1; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 23844435921     PISSN: 08874476     EISSN: None     Source Type: Journal    
DOI: 10.1002/syn.20181     Document Type: Article

References (82)

1. Abdul-Ghani MA, Valiante TA, Pennefather PS. 1996. Sr2+ and quantal events at excitatory synapses between mouse hippocampal neurons in culture. J Physiol 495(Pt 1):113-125.
2. Behr J, Gloveli T, Schmitz D, Heinemann U. 2000. Dopamine depresses excitatory synaptic transmission onto rat subicular neurons via presynaptic D1-like dopamine receptors. J Neurophysiol 84:112-119.
3. Bekkers JM, Clements JD. 1999. Quantal amplitude and quantal variance of strontium-induced asynchronous EPSCs in rat dentate granule neurons. J Physiol 516(Pt 1):227-248.
4. Belleau ML, Warren RA. 2000. Postnatal development of electrophysiological properties of nucleus accumbens neurons. J Neurophysiol 84:2204-2216.
5. Bouron A, Reuter H. 1999. The D1 dopamine receptor agonist SKF-38393 stimulates the release of glutamate in the hippocampus. Neuroscience 94:1063-1070.
6. Breakwell NA, Behnisch T, Publicover SJ, Reymann KG. 1995. Attenuation of high-voltage-activated Ca2+ current run-down in rat hippocampal CA1 pyramidal cells by NaF. Exp Brain Res 106:505-508.
7. 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.
8. Brodie M, Pesold C, Appel S. 1999. Ethanol directly excites dopaminergic ventral tegmental reward neurons. Alcohol clin Exp Res 23:1848-1852.
9. Burgard EC, Hablitz JJ. 1993. NMDA receptor-mediated components of miniature excitatory synaptic currents in developing rat neocortex. J Neurophysiol 70:1841-1852.
10. Calabresi P, Gubellini P, Centonze D, Picconi B, Bernardi G, Chergui K, Svenningsson P, Fienberg AA, Greengard P. 2000. Dopamine and cAMP-regulated phosphoprotein 32 kDa controls both striatal long-term depression and long-term potentiation, opposing forms of synaptic plasticity. J Neurosci 20:8443-8451.
11. Calton JL, Wilson WA, Moore SD. 1998. Magnesium-dependent inhibition of N-methyl-D-aspartate receptor-mediated synaptic transmission by ethanol. J Pharmacol Exp Ther 287:1015-1019.
12. Chen X, Kombian SB, Zidichouski JA, Pittman QJ. 1999. Dopamine depresses glutamatergic synaptic transmission in the rat parabrachial nucleus in vitro. Neuroscience 90:457-468.
13. El-Ghundi M, George S, Drago J, Fletcher P, Fan T, Nguyen T, Liu X, Sibley DR, Westphal H, O'Dowd BF. 1998. Disruption of dopamine D1 receptor gene expression attenuates alcohol-seeking behavior. Eur J Pharmacol 353:149-158.
14. Flint AC, Maisch US, Weishaupt JH, Kriegstein AR, Monyer H. 1997. NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J Neurosci 17:2469-2476.
15. Floresco SB, Blaha CD, Yang CR, Phillips AG. 2001a. Dopamine D1 and NMDA receptors mediate potentiation of basolateral amygdala-evoked firing of nucleus accumbens neurons. J Neurosci 21:6370-6376.
16. Floresco SB, Blaha CD, Yang CR, Phillips AG. 2001b. Modulation of hippocampal and amygdalar-evoked activity of nucleus accumbens neurons by dopamine: cellular mechanisms of input selection. J Neurosci 21:2851-2860.
17. Gonzales RA, Weiss F. 1998. Suppression of ethanol-reinforced behavior by naltrexone is associated with attenuation of the ethanol-induced increase in dialysate dopamine levels in the nucleus accumbens. J Neurosci 18:10663-10671.
18. Harvey J, Lacey MG. 1996. Endogenous and exogenous dopamine depress EPSCs in rat nucleus accumbens in vitro via D1 receptors activation. J Physiol 492(Pt 1):143-154.
19. Harvey J, Lacey MG. 1997. A postsynaptic interaction between dopamine D1 and NMDA receptors promotes presynaptic inhibition in the rat nucleus accumbens via adenosine release. J Neurosci 17:5271-5280.
20. Hendricson AW, Sibbald JR, Morrisett RA. 2004. Ethanol alters the frequency, amplitude, and decay kinetics of Sr2+-supported, asynchronous NMDAR mEPSCs in rat hippocampal slices. J Neurophysiol 91:2568-2577.
21. Hestrin S. 1992. Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature 357:686-689.
22. Hestrin S, Nicoll RA, Perkel DJ, Sah P. 1990. Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J Physiol 422:203-225.
23. Hjelmstad GO. 2004. Dopamine excites nucleus accumbens neurons through the differential modulation of glutamate and GABA release. J Neurosci 24:8621-8628.
24. Hodge CW, Haraguchi M, Erickson H, Samson HH. 1993. Ventral tegmental microinjections of quinpirole decrease ethanol and sucrose-reinforced responding. Alcohol Clin Exp Res 17:370-375.
25. Kerr JN, Wickens JR. 2001. Dopamine D-1/D-5 receptor activation is required for long-term potentiation in the rat neostriatum in vitro. J Neurophysiol 85:117-124.
26. King MM, Huang CY, Chock PB, Nairn AC, Hemmings HC, Jr, Chan KF, Greengard P. 1984. Mammalian brain phosphoproteins as substrates for calcineurin. J Biol Chem 259:8080-8083.
27. Leshner AI, Koob GF. 1999. Drugs of abuse and the brain. Proc Assoc Am Physicians 111:99-108.
28. Levey AI, Hersch SM, Rye DB, Sunahara RK, Niznik HB, Kitt CA, Price DL, Maggio R, Brann MR, Ciliax BJ. 1993. Localization of D1 and D2 dopamine receptors in brain with subtype-specific antibodies. Proc Natl Acad Sci USA 90:8861-8865.
29. Lewis MM, Watts VJ, Lawler CP, Nichols DE, Mailman RB. 1998. Homologous desensitization of the D1A dopamine receptor: efficacy in causing desensitization dissociates from both receptor occupancy and functional potency. J Pharmacol Exp Ther 286:345-353.
30. Li Y, Kauer JA. 2004. Repeated exposure to amphetamine disrupts dopaminergic modulation of excitatory synaptic plasticity and neurotransmission in nucleus accumbens. Synapse 51:1-10.
31. Losi G, Prybylowski K, Fu Z, Luo J, Wenthold RJ, Vicini S. 2003. PSD-95 regulates NMDA receptors in developing cerebellar granule neurons of the rat. J Physiol 548(Pt 1):21-29.
32. Losi G, Vicini S, Neale J. 2004. NAAG fails to antagonize synaptic and extrasynaptic NMDA receptors in cerebellar granule neurons. Neuropharmacology 46:490-496.
33. Lovinger DM. 1995. Developmental decrease in ethanol inhibition of N-methyl-D-aspartate receptors in rat neocortical neurons: relation to the actions of ifenprodil. J Pharmacol Exp Ther 274:164-172.
34. Maldve RE, Zhang TA, Ferrani-Kile K, Schreiber SS, Lippmann MJ, Snyder GL, Fienberg AA, Leslie SW, Gonzales RA, Morrisett RA. 2002. DARPP-32 and regulation of the ethanol sensitivity of NMDA receptors in the nucleus accumbens. Nat Neurosci 5:641-648.
35. Maldve RE, Chen X, Zhang TA, Morrisett RA. 2004. Ethanol selectively inhibits enhanced vesicular release at excitatory synapses: real-time visualization in intact hippocampal slices. Alcohol Clin Exp Res 28:143-152.
36. Martin D, Morrisett RA, Bian XP, Wilson WA, Swartzwelder HS. 1991. Ethanol inhibition of NMDA mediated depolarizations is increased in the presence of Mg2+. Brain Res 546:227-234.
37. Martin G, Ahmed SH, Blank T, Spiess J, Koob GF, Siggins GR. 1999. Chronic morphine treatment alters NMDA receptor-mediated synaptic transmission in the nucleus accumbens. J Neurosci 19:9081-9089.
38. Momiyama T, Sim JA, Brown DA. 1996. Dopamine D1-like receptor-mediated presynaptic inhibition of excitatory transmission onto rat magnocellular basal forebrain neurones. J Physiol 495(Pt 1):97-106.
39. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH. 1994. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
40. Morrisett RA, Martin D, Getting TA, Lewis DV, Wilson WA, Swartzwelder HS. 1991. Ethanol and magnesium ions inhibit N-methyl-D-aspartate-mediated synaptic potentials in an interactive manner. Neuropharmacology 30:1173-1178.
41. Morrisett RA, Swartzwelder HS. 1993. Attenuation of hippocampal long-term potentiation by ethanol: a patch-clamp analysis of glutamatergic and GABAergic mechanisms. J Neurosci 13:2264-2272.
42. Nestler EJ. 2001. Neurobiology. Total recall-the memory of addiction. Science 292:2266-2267.
43. Nicola SM, Malenka RC. 1997. Dopamine depresses excitatory and inhibitory synaptic transmission by distinct mechanisms in the nucleus accumbens. J Neurosci 17:5697-5710.
44. Nie Z, Madamba SG, Siggins GR. 1994. Ethanol inhibits glutamatergic neurotransmission in nucleus accumbens neurons by multiple mechanisms. J Pharmacol Exp Ther 271:1566-1573.
45. Nie Z, Schweitzer P, Roberts AJ, Madamba SG, Moore SD, Siggins GR. 2004. Ethanol augments GABAergic transmission in the central amygdala via CRF1 receptors. Science 303:1512-1514.
46. Oliet SH, Malenka RC, Nicoll RA. 1996. Bidirectional control of quantal size by synaptic activity in the hippocampus. Science 271:1294-1297.
47. Panchalingam S, Undie AS. 2000. Optimized binding of [35S] GTPgammaS to Gq-like proteins stimulated with dopamine D1-like receptor agonists. Neurochem Res 25:759-767.
48. Partridge JG, Tang KC, Lovinger DM. 2000. Regional and postnatal heterogeneity of activity-dependent long-term changes in synaptic efficacy in the dorsal striatum. J Neurophysiol 84:1422-1429.
49. Pennartz CM, Dolleman-Van der Weel MJ, Kitai ST, Lopes da Silva FH. 1992. Presynaptic dopamine D1 receptors attenuate excitatory and inhibitory limbic inputs to the shell region of the rat nucleus accumbens studied in vitro. J Neurophysiol 67:1325-1334.
50. Pennartz CM, Ameerun RF, Groenewegen HJ, Lopes da Silva FH. 1993. Synaptic plasticity in an in vitro slice preparation of the rat nucleus accumbens. Eur J Neurosci 5:107-117.
51. Pennartz CM, Groenewegen HJ, Lopes da Silva FH. 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.
52. Perouansky M, Yaari Y. 1993. Kinetic properties of NMDA receptor-mediated synaptic currents in rat hippocampal pyramidal cells versus interneurones. J Physiol (Lond) 465:223-244.
53. Portera Cailliau C, Price DL, Martin LJ. 1996. N-methyl-D-aspartate receptor proteins NR2A and NR2B are differentially distributed in the developing rat central nervous system as revealed by subunit-specific antibodies. J Neurochem 66:692-700.
54. Rassnick S, Pulvirenti L, Koob GF. 1993. SDZ-205,152, a novel dopamine receptor agonist, reduces oral ethanol self-administration in rats. Alcohol 10:127-132.
55. Reynolds JN, Hyland BI, Wickens JR. 2001. A cellular mechanism of reward-related learning. Nature 413:67-70.
56. Risinger FO, Freeman PA, Greengard P, Fienberg AA. 2001. Motivational effects of ethanol in DARPP-32 knock-out mice. J Neurosci 21:340-348.
57. Roberto M, Schweitzer P, Madamba SG, Stouffer DG, Parsons LH, Siggins GR. 2004. Acute and chronic ethanol alter glutamatergic transmission in rat central amygdala: an in vitro and in vivo analysis. J Neurosci 24:1594-1603.
58. Rohrbough J, Spitzer NC. 1999. Ca(2+)-permeable AMPA receptors and spontaneous presynaptic transmitter release at developing excitatory spinal synapses. J Neurosci 19:8528-8541.
59. Samson HH, Hodge CW, Tolliver GA, Haraguchi M. 1993. Effect of dopamine agonists and antagonists on ethanol-reinforced behavior: the involvement of the nucleus accumbens. Brain Res Bull 30:133-141.
60. Schramm NL, Egli RE, Winder DG. 2002. LTP in the mouse nucleus accumbens is developmentally regulated. Synapse 45:213-219.
61. 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.
62. 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.
63. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY. 1994. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368:144-147.
64. Snyder GL, Fienberg AA, Huganir RL, Greengard P. 1998. A dopamine/D1 receptor/protein kinase A/dopamine- and cAMP-regulated phosphoprotein (Mr 32 kDa)/protein phosphatase-1 pathway regulates dephosphorylation of the NMDA receptor. J Neurosci 18:10297-10303.
65. Spanagel R, Weiss F. 1999. The dopamine hypothesis of reward: past and current status. Trends Neurosci 22:521-527.
66. Thomas MP, Monaghan DT, Morrisett RA. 1998. Evidence for a causative role of N-methyl-D-aspartate receptors in an in vitro model of alcohol withdrawal hyperexcitability. J Pharmacol Exp Ther 287:87-97.
67. Undie AS, Friedman E. 1990. Stimulation of a dopamine D1 receptor enhances inositol phosphates formation in rat brain. J Pharmacol Exp Ther 253:987-992.
68. Ungless MA, Whistler JL, Malenka RC, Bonci A. 2001. Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411:583-587.
69. Van der Kloot W. 1991. The regulation of quantal size. Prog Neurobiol 36:93-130.
70. Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB, Grayson DR. 1998. Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J Neurophysiol 79:555-566.
71. Vorel SR, Liu X, Hayes RJ, Spector JA, Gardner EL. 2001. Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 292:1175-1178.
72. Wang Z, Feng XQ, Zheng P. 2002. Activation of presynaptic D1 dopamine receptors by dopamine increases the frequency of spontaneous excitatory postsynaptic currents through protein kinase A and protein kinase C in pyramidal cells of rat prelimbic cortex. Neuroscience 112:499-508.
73. 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.
74. Wenzel A, Fritschy JM, Mohler H, Benke D. 1997. NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins. J Neurochem 68:469-478.
75. Williams K, Russell SL, Shen YM, Molinoff PB. 1993. Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro. Neuron 10:267-278.
76. Yamamoto Y, Nakanishi H, Takai N, Shimazoe T, Watanabe S, Kita H. 1999. Expression of N-methyl-D-aspartate receptor-dependent long-term potentiation in the neostriatal neurons in an in vitro slice after ethanol withdrawal of the rat. Neuroscience 91:59-68.
77. Yang SN. 1999. Presynaptic involvement of nitric oxide in dopamine D1/D5 receptor-induced sustained enhancement of synaptic currents mediated by ionotropic glutamate receptors in the rat hippocampus. Neurosci Lett 270:87-90.
78. Yim HJ, Schauert T, Randall PK, Gonzales RA. 1998. Comparison of local and systemic ethanol effects on extracellular dopamine concentration in rat nucleus accumbens by microdialysis. Alcohol Clin Exp Res 22:367-374.
79. Zhang TA, Rakhilin SV, Fienberg AA, Nairn AC, Greengard P, Morrisett RA. 2005. Analysis of D1 modulation of ethanol sensitivity of NMDA EPSCs in the nucleus accumbens of RCS knockout mice. Research Society of Alcoholism abstract.
80. Zhong J, Russell SL, Pritchett DB, Molinoff PB, Williams K. 1994. Expression of mRNAs encoding subunits of the N-methyl-D-aspartate receptor in cultured cortical neurons. Mol Pharmacol 45:846-853.
81. Zhou FM, Hablitz JJ. 1997. Rapid kinetics and inward rectification of miniature EPSCs in layer I neurons of rat neocortex. J Neurophysiol 77:2416-2426.
82. Ziskind-Conhaim L, Gao BX, Hinckley C. 2003. Ethanol dual modulatory actions on spontaneous postsynaptic currents in spinal motoneurons. J Neurophysiol 89:806-813.