Involvement of non-NMDA glutamate receptors in central amygdala in synaptic actions of ethanol and ethanol-induced reward behavior

Journal of Neuroscience

Volumn 27, Issue 2, 2007, Pages 289-298

  Zhu, Wei ^a   Bie, Bihua ^a   Pan, Zhizhong Z ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Alcohol addiction; AMPA receptors; Conditioned place preference; Drug abuse; EPSCs; Whole cell recording

Indexed keywords

ALCOHOL; CALCIUM CHANNEL N TYPE; GLUTAMATE RECEPTOR; GLUTAMIC ACID; POSTSYNAPTIC RECEPTOR; PRESYNAPTIC RECEPTOR;

ALCOHOLISM; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; EMOTION; EVOKED RESPONSE; IN VITRO STUDY; LEARNING; MALE; NONHUMAN; PLACE PREFERENCE; POSTSYNAPTIC INHIBITION; PRESYNAPTIC INHIBITION; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; REINFORCEMENT; REWARD; SYNAPSE; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP; WHOLE CELL;

AMYGDALA; ANIMALS; ETHANOL; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; RATS; RATS, WISTAR; RECEPTORS, GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; REWARD; SYNAPTIC TRANSMISSION;

EID: 33846225080     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3912-06.2007     Document Type: Article

References (62)

1. Akinshola BE, Yasuda RP, Peoples RW, Taylor RE (2003) Ethanol sensitivity of recombinant homomeric and heteromeric AMPA receptor subunits expressed in Xenopus oocytes. Alcohol Clin Exp Res 27:1876-1883.
2. Baxter MG, Murray EA (2002) The amygdala and reward. Nat Rev Neurosci 3:563-573.
3. Biala G, Kotlinska J (1999) Blockade of the acquisition of ethanol-induced conditioned place preference by N-methyl-D- aspartate receptor antagonists. Alcohol Alcohol 34:175-182.
4. Bie B, Peng Y, Zhang Y, Pan ZZ (2005) cAMP-mediated mechanisms for pain sensitization during opioid withdrawal. J Neurosci 25:3824-3832.
5. Bienkowski P, Kuca P, Piasecki J, Kostowski W (1996) Low dose of ethanol induces conditioned place preference in rats after repeated exposures to ethanol or saline injections. Alcohol Alcohol 31:547-553.
6. Bozarth MA (1990) Evidence for the rewarding effects of ethanol using the conditioned place preference method. Pharmacol Biochem Behav 35:485-487.
7. 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.
8. Carpenter-Hyland EP, Woodward JJ, Chandler LJ (2004) Chronic ethanol induces synaptic but not extrasynaptic targeting of NMDA receptors. J Neurosci 24:7859-7868.
9. Carta M, Ariwodola OJ, Weiner JL, Valenzuela CF (2003) Alcohol potently inhibits the kainate receptor-dependent excitatory drive of hippocampal interneurons. Proc Natl Acad Sci USA 100:6813-6818.
10. Chandler LJ, Sutton G, Norwood D, Sumners C, Crews FT (1997) Chronic ethanol increases N-methyl-D-aspartate-stimulated nitric oxide formation but not receptor density in cultured cortical neurons. Mol Pharmacol 51:733-740.
11. Chen X, Michaelis ML, Michaelis EK (1997) Effects of chronic ethanol treatment on the expression of calcium transport carriers and NMDA/glutamate receptor proteins in brain synaptic membranes. J Neurochem 69:1559-1569.
12. Criswell HE, Ming Z, Griffith BL, Breese GR (2003) Comparison of effect of ethanol on N-methyl-D-aspartate- and GABA-gated currents from acutely dissociated neurons: absence of regional differences in sensitivity to ethanol. J Pharmacol Exp Ther 304:192-199.
13. Cunningham CL, Henderson CM, Bormann NM (1998) Extinction of ethanol-induced conditioned place preference and conditioned place aversion: effects of naloxone. Psychopharmacology (Berl) 139:62-70.
14. Cunningham CL, Ferree NK, Howard MA (2003) Apparatus bias and place conditioning with ethanol in mice. Psychopharmacology (Berl) 170:409-422.
15. Dildy-Mayfield JE, Harris RA (1992) Comparison of ethanol sensitivity of rat brain kainate, DL-alpha-amino-3-hydroxy-5-methyl-4-isoxalone proprionic acid and N-methyl-D-aspartate receptors expressed in Xenopus oocytes. J Pharmacol Exp Ther 262:487-494.
16. Dobrunz LE, Stevens CF (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18:995-1008.
17. Fadda F, Rossetti ZL (1998) Chronic ethanol consumption: from neuroadaptation to neurodegeneration. Prog Neurobiol 56:385-431.
18. Ferreira VM, Frausto S, Browning MD, Savage DD, Morato, Gs, Valenzuela CF (2001) Ionotropic glutamate receptor subunit expression in the rat hippocampus: lack of an effect of a long-term ethanol exposure paradigm. Alcohol Clin Exp Res 25:1536-1541.
19. Floyd DW, Jung KY, McCool BA (2003) Chronic ethanol ingestion facilitates N-methyl-D-aspartate receptor function and expression in rat lateral/basolateral amygdala neurons. J Pharmacol Exp Ther 307:1020-1029.
20. Follesa P, Ticku MK (1996) Chronic ethanol-mediated up-regulation of the N-methyl-D-aspartate receptor polypeptide subunits in mouse cortical neurons in culture. J Biol Chem 271:13297-13299.
21. Gottfried JA, O'Doherty J, Dolan RJ (2003) Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301:1104-1107.
22. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
23. Honse Y, Ren H, Lipsky RH, Peoples RW (2004) Sites in the fourth membrane-associated domain regulate alcohol sensitivity of the NMDA receptor. Neuropharmacology 46:647-654.
24. Hyytia P, Koob GF (1995) GABAA receptor antagonism in the extended amygdala decreases ethanol self-administration in rats. Eur J Pharmacol 283:151-159.
25. Koob GF (2004) A role for GABA mechanisms in the motivational effects of alcohol. Biochem Pharmacol 68:1515-1525.
26. Koob GF, Sanna PP, Bloom FE (1998) Neuroscience of addiction. Neuron 21:467-476.
27. Krystal JH, Petrakis IL, Mason G, Trevisan L, D'Souza DC (2003) N-methyl-D-aspartate glutamate receptors and alcoholism: reward, dependence, treatment, and vulnerability. Pharmacol Ther 99:79-94.
28. Kumari M (2001) Differential effects of chronic ethanol treatment on N-methyl-D-aspartate R1 splice variants in fetal cortical neurons. J Biol Chem 276:29764-29771.
29. Lovinger DM, White G, Weight FF (1989) Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 243:1721-1724.
30. Ma J, Pan ZZ (2006) Contribution of brainstem GABA(A) synaptic transmission to morphine analgesic tolerance. Pain 122:163-173.
31. Maccaferri G, Dingledine R (2002) Complex effects of CNQX on CA1 interneurons of the developing rat hippocampus. Neuropharmacology 43:523-529.
32. Mameli M, Zamudio PA, Carta M, Valenzuela CF (2005) Developmentally regulated actions of alcohol on hippocampal glutamatergic transmission. J Neurosci 25:8027-8036.
33. Masood K, Wu C, Brauneis U, Weight FF (1994) Differential ethanol sensitivity of recombinant N-methyl-D-aspartate receptor subunits. Mol Pharmacol 45:324-329.
34. Matsuzawa S, Suzuki T, Misawa M, Nagase H (1999) Different roles of mu-, delta- and kappa-opioid receptors in ethanol-associated place preference in rats exposed to conditioned fear stress. Eur J Pharmacol 368:9-16.
35. Mead AN, Stephens DN (2003) Involvement of AMPA receptor GluR2 subunits in stimulus-reward learning: evidence from glutamate receptor gria2 knock-out mice. J Neurosci 23:9500-9507.
36. 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.
37. Moykkynen T, Korpi ER, Lovinger DM (2003) Ethanol inhibits alpha-amino-3-hydyroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor function in central nervous system neurons by stabilizing desensitization. J Pharmacol Exp Ther 306:546-555.
38. Narahashi T, Kuriyama K, Illes P, Wirkner K, Fischer W, Muhlberg K, Scheibler P, Allgaier C, Minami K, Lovinger D, Lallemand F, Ward RJ, DeWitte P, Itatsu T, Takei Y, Oide H, Hirose M, Wang XE, Watanabe S, Tateyama M, et al. (2001) Neuroreceptors and ion channels as targets of alcohol. Alcohol Clin Exp Res 25:182S-188S.
39. Nestler EJ (2001) Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci 2:119-128.
40. 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.
41. 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.
42. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, Ed 2. Sydney: Academic.
43. Roberto M, Madamba SG, Moore SD, Tallent MK, Siggins GR (2003) Ethanol increases GABAergic transmission at both pre- and postsynaptic sites in rat central amygdala neurons. Proc Natl Acad Sci USA 100:2053-2058.
44. 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.
45. Roberto M, Bajo M, Crawford E, Madamba SG, Siggins GR (2005) Chronic ethanol exposure and protracted abstinence alter NMDA receptors in central amygdala. Neuropsychopharmacology 31:988-996.
46. Rudolph JG, Walker DW, Iimuro Y, Thurman RG, Crews FT (1997) NMDA receptor binding in adult rat brain after several chronic ethanol treatment protocols. Alcohol Clin Exp Res 21:1508-1519.
47. Sanchis-Segura C, Borchardt T, Vengeliene V, Zghoul T, Bachteler D, Gass P, Sprengel R, Spanagel R (2006) Involvement of the AMPA receptor GluR-C subunit in alcohol-seeking behavior and relapse. J Neurosci 26:1231-1238.
48. See RE, Fuchs RA, Ledford CC, McLaughlin J (2003) Drug addiction, relapse, and the amygdala. Ann NY Acad Sci 985:294-307.
49. Siggins GR, Martin G, Roberto M, Nie Z, Madamba S, De Lecea L (2003) Glutamatergic transmission in opiate and alcohol dependence. Ann NY Acad Sci 1003:196-211.
50. Siggins GR, Roberto M, Nie Z (2005) The tipsy terminal: presynaptic effects of ethanol. Pharmacol Ther 107:80-98.
51. Smothers CT, Woodward JJ (2006) Effects of amino acid substitutions in transmembrane domains of the NR1 subunit on the ethanol inhibition of recombinant N-methyl-D-aspartate receptors. Alcohol Clin Exp Res 30:523-530.
52. Steffensen SC, Nie Z, Criado JR, Siggins GR (2000) Ethanol inhibition of N-methyl-D-aspartate responses involves presynaptic gamma-aminobutyric acid(B) receptors. J Pharmacol Exp Ther 294:637-647.
53. Tabakoff B, Hoffman PL (1996) Alcohol addiction: an enigma among us. Neuron 16:909-912.
54. Trevisan L, Fitzgerald LW, Brose N, Gasic GP, Heinemann SF, Duman RS, Nestler EJ (1994) Chronic ingestion of ethanol up-regulates NMDAR1 receptor subunit immunoreactivity in rat hippocampus. J Neurochem 62:1635-1638.
55. Trujillo KA, Akil H (1991) Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science 251:85-87.
56. Tzschentke TM (1998) Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog Neurobiol 56:613-672.
57. 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.
58. Weiner JL, Dunwiddie TV, Valenzuela CF (1999) Ethanol inhibition of synaptically evoked kainate responses in rat hippocampal CA3 pyramidal neurons. Mol Pharmacol 56:85-90.
59. Woodward JJ (2000) Ethanol and NMDA receptor signaling. Crit Rev Neurobiol 14:69-89.
60. Wright JM, Peoples RW, Weight FF (1996) Single-channel and whole-cell analysis of ethanol inhibition of NMDA-activated currents in cultured mouse cortical and hippocampal neurons. Brain Res 738:249-256.
61. Zhu W, Pan ZZ (2004) Synaptic properties and postsynaptic opioid effects in rat central amygdala neurons. Neuroscience 127:871-879.
62. Zhu W, Pan ZZ (2005) Mu-opioid-mediated inhibition of glutamate synaptic transmission in rat central amygdala neurons. Neuroscience 133:97-103.