Long-lasting alterations in membrane properties, K + currents, and glutamatergic synaptic currents of nucleus accumbens medium spiny neurons in a rat model of alcohol dependence

Frontiers in Neuroscience

Volumn , Issue JUN, 2012, Pages

  Marty, Vincent N ^a   Spigelman, Igor ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alcoholism; Chronic intermittent ethanol treatment; GluA2 lacking AMPARs; Reward; Synaptic transmission; Withdrawal

Indexed keywords

ALCOHOL; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; POTASSIUM CHANNEL;

ACTION POTENTIAL; ALCOHOL WITHDRAWAL; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONDUCTANCE; CONTROLLED STUDY; MALE; NERVE CELL; NONHUMAN; NUCLEUS ACCUMBENS; POTASSIUM CURRENT; RAT; SYNAPSE; SYNAPTIC POTENTIAL;

EID: 84862657141     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2012.00086     Document Type: Article

References (81)

1. Abriam, A., Finzen, E., Bito-Onon, J., Liang, J., Olsen, R. W., and Spigelman, I. (2009). Dose- and frequency dependence of cross-tolerance to diazepam after chronic intermittent ethanol treatment of rats. Abstr. Soc. Neurosci. 34, 64.66.
2. Belleau, M. L., and Warren, R. A. (2000). Postnatal development of electro-physiological properties of nucleus accumbens neurons. J. Neurophysiol. 84,2204-2216.
3. Benke, T. A., Luthi, A., Isaac, J. T., and Collingridge, G. L. (1998). Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393, 793-797.
4. Benke, T. A., Luthi, A., Palmer, M. J., Wikstrom, M. A., Anderson, W. W., Isaac, J. T., and Collingridge, G. L. (2001). Mathematical modelling of non-stationary fluctuation analysis for studying channel properties of synaptic AMPA receptors. J. Physiol. (Lond.) 537, 407-420.
5. Blomeley, C. P., Cains, S., Smith, R., and Bracci, E. (2011). Ethanol affects striatal interneurons directly and projection neurons through a reduction in cholinergic tone. Neuropsy-chopharmacology 36, 1033-1046.
6. Boudreau, A. C., Reimers, J. M., Milo-vanovic, M., and Wolf, M. E. (2007). Cell surface AMPA receptors in the rat nucleus accumbens increase during cocaine withdrawal but internalize after cocaine challenge in association with altered activation of mitogen-activated protein kinases. J. Neurosci. 27,10621-10635.
7. Boudreau,A.C.,and Wolf, M.E. (2005). Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens. J. Neurosci. 25, 9144-9151.
8. Budelli,G.,Hage,T.A.,Wei,A.,Rojas,P., Jong, Y. J., O'Malley, K., and Salkoff, L. (2009). Na+-activated K+ channels express a large delayed outward current in neurons during normal physiology. Nat. Neurosci. 12, 745-750.
9. Buldakova, S. L., Kim, K. K., Tikhonov, D. B., and Magazanik, L. G. (2007). Selective blockade of Ca2+ permeable AMPA receptors in CA1 area of rat hippocampus. Neuroscience 144, 88-99.
10. Cagetti, E., Liang, J., Spigelman, I., and Olsen, R. W (2003). Withdrawal from chronic intermittent ethanol treatment changes subunit composition, reduces synaptic function, and decreases behavioral responses to positive allosteric modulators of GABAA receptors. Mol. Pharmacol. 63, 53-64.
11. Chaudhri, N., Sahuque, L. L., Schairer, W. W., and Janak, P. H. (2010). Separable roles of the nucleus accumbens core and shell in context- and cue-induced alcohol-seeking. Neuropsy-chopharmacology 35, 783-791.
12. Conrad, K. L., Tseng, K. Y., Uejima, J. L., Reimers, J. M., Heng, L. J., Sha-ham, Y., Marinelli, M., and Wolf, M. E. (2008). Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 454, 118-121.
13. Cuzon Carlson, V. C., Seabold, G. K., Helms, C. M., Garg, N., Oda-giri, M., Rau, A. R., Daunais, J., Alvarez, V. A., Lovinger, D. M., and Grant, K. A. (2011). Synaptic and morphological neuroadaptations in the putamen associated with long-term, relapsing alcohol drinking in primates. Neuropsychopharmacology 36, 2513-2528.
14. Deng, P., Pang, Z. P., Lei, Z., Shikano, S., Xiong, Q., Harvey, B. K., London, B., Wang, Y., Li, M., and Xu, Z. C. (2011). Up-regulation of A-type potassium currents protects neurons against cerebral ischemia. J. Cereb. Blood Flow Metab. 31, 1823-1835.
15. Ferrario, C. R., Loweth, J. A., Milo-vanovic, M., Ford, K. A., Galinanes, G. L., Heng, L. J., Tseng, K. Y., and Wolf, M. E. (2011). Alterations in AMPA receptor subunits and TARPs in the rat nucleus accumbens related to the formation of Ca(2+)-permeable AMPA receptors during the incubation of cocaine craving. Neuropharmacology 61, 1141-1151.
16. Floresco, S. B., Todd, C. L., and Grace, A. A. (2001). Glutamatergic affer-ents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons. J. Neurosci. 21, 4915-4922.
17. Gertler, T. S., Chan, C. S., and Surmeier, D. J. (2008). Dichotomous anatomical properties of adult striatal medium spiny neurons. J. Neurosci. 28, 10814-10824.
18. Ghasemzadeh, M. B., Mueller, C., and Vasudevan, P. (2009). Behavioral sensitization to cocaine is associated with increased glutamate receptor trafficking to the postsynaptic density after extended withdrawal period. Neuroscience 159,414-426.
19. Goto, Y., and O'Donnell, P. (2001). Synchronous activity in the hippocampus and nucleus accumbens in vivo. I Neurosd. 21, RC131.
20. Gruber, A. J., and O'Donnell, P. (2009). Bursting activation of prefrontal cortex drives sustained up states in nucleus accumbens spiny neurons in vivo. Synapse 63,173-180.
21. Guire, E. S., Oh, M. C., Soderling, T. R., and Derkach, V. A. (2008). Recruitment of calcium-permeable AMPA receptors during synaptic potentia-tion is regulated by CaM-kinase I. J. Neurosci. 28, 6000-6009.
22. Hartveit, E., and Veruki, M. L. (2007). Studying properties of neurotrans-mitter receptors by non-stationary noise analysis of spontaneous postsynaptic currents and agonist-evoked responses in outside-out patches. Nat. Protoc. 2,434-448.
23. Hopf, F. W., Bowers, M. S., Chang, S. J., Chen, B. T., Martin, M., Seif, T., Cho, S. L., Tye, K., and Bonci, A. (2010). Reduced nucleus accumbens SK channel activity enhances alcohol seeking during abstinence. Neuron 65, 682-694.
24. Howland, J. G., Taepavarapruk, P., and Phillips, A. G. (2002). Glutamate receptor-dependent modulation of dopamine efflux in the nucleus accumbens by basolateral, but not central, nucleus of the amygdala in rats.J. Neurosci. 22, 1137-1145.
25. Hughes, J. C., and Cook, C. C. (1997). The efficacy of disulfiram: a review of outcome studies. Addiction 92, 381-395.
26. Hyman, S. E., Malenka, R. C., and Nestler, E. J. (2006). Neural mechanisms of addiction: the role of reward-related learning and memory. Annu. Rev. Neurosci. 29, 565-598.
27. Isaac, J. T., Ashby, M. C., and Mcbain, C. J. (2007). The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54, 859-871.
28. Ishikawa, M., Mu, P., Moyer, J. T., Wolf, J. A., Quock, R. M., Davies, N. M., Hu, X. T., Schluter, O. M., and Dong, Y. (2009). Homeostatic synapse-driven membrane plasticity in nucleus accumbens neurons. J. Neurosci. 29, 5820-5831.
29. Jeanes, Z. M., Buske, T. R., and Morrisett, R. A. (2011). In vivo chronic intermittent ethanol exposure reverses the polarity of synaptic plasticity in the nucleus accumbens shell. J. Pharmacol. Exp. Ther. 336, 155-164.
30. Johnson, M. W., Chotiner, J. K., and Watson, J. B. (1997). Isolation and characterization of synaptoneuro-somes from single rat hippocam-pal slices. J. Neurosci. Methods 77, 151-156.
31. Ju,W.,Morishita,W.,Tsui,J.,Gaietta,G., Deerinck, T. J., Adams, S. R., Garner, C. C., Tsien, R. Y., Ellisman, M. H., and Malenka, R. C. (2004). Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat. Neurosci. 7,244-253.
32. Kasanetz, F., Deroche-Gamonet, V., Berson, N., Balado, E., Lafourcade, M., Manzoni, O., and Piazza, P. V. (2010). Transition to addiction is associated with a persistent impairment in synaptic plasticity. Science 328,1709-1712.
33. Kim, J., Park, B. H., Lee, J. H., Park, S. K., and Kim, J. H. (2011). Cell type-specific alterations in the nucleus accumbens by repeated exposures to cocaine. Biol. Psychiatry 69, 1026-1034.
34. Kokka, N., Sapp, D. W., Taylor, A. M., and Olsen, R. W (1993). The kindling model of alcohol dependence: similar persistent reduction in seizure threshold to pentylenete-trazol in animals receiving chronic ethanol or chronic pentylenetetra-zol. Alcohol. Clin. Exp. Res. 17, 525-531.
35. Koob, G. F. (2008). Hedonic homeostatic dysregulation as a driver of drug-seeking behavior. DrugDiscov. Today Dis. Models 5,207-215.
36. Koob, G. F., Ahmed, S. H., Boutrel, B., Chen, S. A., Kenny, P. J., Markou, A., O'Dell, L. E., Parsons, L. H., and Sanna, P. P. (2004). Neurobiolog-ical mechanisms in the transition from drug use to drug dependence. Neurosci. Biobehav. Rev. 27,739-749.
37. Koob, G. F., and Le Moal, M. (2008). Review. Neurobiological mechanisms for opponent motivational processes in addiction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 3113-3123.
38. Lack, A. K., Diaz, M. R., Chappell, A., Dubois, D. W., and Mccool, B. A. (2007). Chronic ethanol and withdrawal differentially modulate pre-and postsynaptic function at glu-tamatergic synapses in rat basolateral amygdala. J. Neurophysiol. 98, 3185-3196.
39. LaLumiere, R. T., and Kalivas, P. W. (2008). Glutamate release in the nucleus accumbens core is necessary for heroin seeking. J. Neurosci. 28, 3170-3177.
40. Liang, J., Suryanarayanan, A., Abriam, A., Snyder, B., Olsen, R. W., and Spigelman, I. (2007). Mechanisms of reversible GABAA receptor plasticity after ethanol intoxication. J. Neurosci. 27,12367-12377.
41. Liang, J., Zhang, N., Cagetti, E., Houser, C. R., Olsen, R. W., and Spigelman, I. (2006). Chronic intermittent ethanol-induced switch of ethanol actions from extrasynaptic to synaptic hippocampal GABAA receptors. J. Neurosci. 26, 1749-1758.
42. Magazanik, L. G., Buldakova, S. L., Samoilova, M. V., Gmiro, V. E., Mel-lor, I. R., and Usherwood, P. N. (1997). Block of open channels of recombinant AMPA receptors and native AMPA/kainate receptors by adamantane derivatives. J. Physiol. (Lond.) 505(Pt 3), 655-663.
43. Mameli, M., Balland, B., Lujan, R., and Luscher, C. (2007). Rapid synthesis and synaptic insertion of GluR2 for mGluR-LTD in the ventral tegmen-tal area. Science 317, 530-533.
44. Mameli, M., Halbout, B., Creton, C., Engblom, D., Parkitna, J. R., Spanagel, R., and Luscher, C. (2009). Cocaine-evoked synaptic plasticity: persistence in the VTA triggers adaptations in the NAc. Nat. Neurosci. 12, 1036-1041.
45. Mann, K., Lehert, P., and Morgan, M. Y. (2004). The efficacy of acamprosate in the maintenance of abstinence in alcohol-dependent individuals: results of a meta-analysis. Alcohol. Clin. Exp. Res. 28,51-63.
46. Mermelstein, P. G., Song, W J., Tkatch, T., Yan, Z., and Surmeier, D. J. (1998). Inwardly rectifying potassium (IRK) currents are correlated with IRK subunit expression in rat nucleus accumbens medium spiny neurons. J. Neurosci. 18,6650-6661.
47. Mu, P., Moyer, J. T., Ishikawa, M., Zhang, Y., Panksepp, J., Sorg, B. A., Schluter, O. M., and Dong, Y. (2010). Exposure to cocaine dynamically regulates the intrinsic membrane excitability of nucleus accumbens neurons. J. Neurosci. 30, 3689-3699.
48. Mulholland, P. J., Becker, H. C., Woodward, J. J., and Chandler, L. J. (2011). Small conductance calcium-activated potassium type 2 channels regulate alcohol-associated plasticity of glutamatergic synapses. Biol. Psychiatry 69, 625-632.
49. Mulligan, M. K., Rhodes, J. S., Crabbe, J. C., Mayfield, R. D., Adron Harris, R., and Ponomarev, I. (2011). Molecular profiles of drinking alcohol to intoxication in C57BL/6J mice. Alcohol. Clin. Exp. Res. 35, 659-670.
50. Neasta, J., Ben Hamida, S., Yowell, Q., Carnicella, S., and Ron, D. (2010). Role for mammalian target of rapamycin complex 1 signaling in neuroadaptations underlying alcohol-related disorders. Proc. Natl. Acad. Sci. U.S.A. 107, 20093-20098.
51. Neasta, J., Ben Hamida, S., Yowell, Q. V., Carnicella, S., and Ron, D. (2011). AKT signaling pathway in the nucleus accumbens mediates excessive alcohol drinking behaviors. Biol. Psychiatry 70, 575-582.
52. Nestler, E. J. (2001). Molecular neurobi-ology of addiction. Am. J. Addict. 10, 201-217.
53. Nie, Z., Madamba, S. G., and Sig-gins, G. R. (1994). Ethanol inhibits glutamatergic neurotransmission in nucleus accumbens neurons by multiple mechanisms. J. Pharmacol. Exp. Ther. 271, 1566-1573.
54. Nisenbaum, E. S., and Wilson, C. J. (1995). Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J. Neurosci. 15, 4449-4463.
55. Nisenbaum, E. S., Xu, Z. C., and Wilson, C.J. (1994). Contribution of aslowly inactivating potassium current to the transition to firing of neostriatal spiny projection neurons. J. Neurophysiol. 71, 1174-1189.
56. O'Donnell, P., and Grace, A. A. (1993). Physiological and morphological properties of accumbens core and shell neurons recorded in vitro. Synapse 13, 135-160.
57. O'Donnell, P., and Grace, A. A. (1995). Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of pre-frontal cortical input. J. Neurosci. 15, 3622-3639.
58. Olive, M. F., Cleva, R. M., Kalivas, P. W., and Malcolm, R. J. (2012). Glutamatergic medications for the treatment of drug and behavioral addictions. Pharmacol. Biochem. Behav. 100,801-810.
59. Rassnick, S., Pulvirenti, L., and Koob, G. E (1992). Oral ethanol self-administration in rats is reduced by the administration of dopamine and glutamate receptor antagonists into the nucleus accumbens. Psychopharmacology (Berl.) 109, 92-98.
60. Rehm, J., Mathers, C., Popova, S., Thavorncharoensap, M., Teer-awattananon, Y., and Patra, J. (2009). Global burden of disease and injury and economic cost attributable to alcohol use and alcohol-use disorders. Lancet 373, 2223-2233.
61. Rimondini, R., Sommer, W., and Heilig, M. (2003). A temporal threshold for induction of persistent alcohol preference: behavioral evidence in a rat model of intermittent intoxication. J. Stud. Alcohol 64, 445-449.
62. Ross, S., and Peselow, E. (2009). Pharmacotherapy of addictive disorders. Clin. Neuropharmacol. 32, 277-289.
63. Sears, R. M., Liu, R. J., Narayanan, N. S., Sharf, R., Yeckel, M. F., Laubach, M., Aghajanian, G. K., and Dileone, R. J. (2010). Regulation of nucleus accumbens activity by the hypothalamic neuropeptide melanin-concentrating hormone. J. Neurosci. 30, 8263-8273.
64. Sesack, S. R., and Grace, A. A. (2010). Cortico-Basal Ganglia reward network: microcircuitry. Neuropsychopharmacology 35, 27-47.
65. Shao, L. R., Halvorsrud, R., Borg-Graham, L., and Storm, J. E (1999). The role of BK-type Ca2+-dependent K+ channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. J. Physiol. (Lond.) 521(Pt 1), 135-146.
66. Shen, W., Tian, X., Day, M., Ulrich, S., Tkatch, T., Nathanson, N. M., and Surmeier, D. J. (2007). Cholinergic modulation of Kir2 channels selectively elevates dendritic excitability in striatopalli-dal neurons. Nat. Neurosci. 10, 1458-1466.
67. Snyder, J. L., and Bowers, T. G. (2008). The efficacy of acamprosate and nal-trexone in the treatment of alcohol dependence: a relative benefits analysis of randomized controlled trials. Am. J. Drug Alcohol Abuse 34, 449-461.
68. Steephen, J. E., and Manchanda, R. (2009). Differences in biophysical properties of nucleus accumbens medium spiny neurons emerging from inactivation of inward rectifying potassium currents. J. Comput. Neurosci. 27, 453-470.
69. Stern, E. A., Kincaid, A. E., and Wilson, C. J. (1997). Spontaneous subthresh-old membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J. Neurophysiol. 77, 1697-1715.
70. Stuber, G. D., Hopf, F. W., Tye, K. M., Chen, B. T., and Bonci, A. (2010). Neuroplastic alterations in the lim-bic system following cocaine or alcohol exposure. Curr. Top. Behav. Neurosci. 3, 3-27.
71. Sutton, M. A., Ito, H. T., Cressy, P., Kempf, C., Woo, J. C., and Schuman, E. M. (2006). Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 125, 785-799.
72. Szumlinski, K. K., Ary, A. W., Lominac, K. D., Klugmann, M., and Kippin, T. E. (2008). Accumbens Homer2 overexpression facilitates alcohol-induced neuroplasticity in C57BL/6J mice. Neuropsychopharmacology 33, 1365-1378.
73. Szumlinski, K. K., Lominac, K. D., Ole-son, E. B., Walker, J. K., Mason, A., Dehoff, M. H., Klugmann, M., Cagle, S., Welt, K., During, M., Worley P. E, Middaugh, L. D., and Kalivas, P. W (2005). Homer2 is necessary for EtOH-induced neuroplasticity. J. Neurosci. 25,7054-7061.
74. Thiagarajan, T. C., Lindskog, M., and Tsien, R. W (2005). Adaptation to synaptic inactivity in hippocampal neurons. Neuron 47, 725-737.
75. Thomas, M. J., Beurrier, C., Bonci, A., and Malenka, R. C. (2001). Long-term depression in the nucleus accumbens: a neural correlate of behavioral sensitization to cocaine. Nat. Neurosci. 4, 1217-1223.
76. Turrigiano, G. G. (2008). The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135, 422-435.
77. Uchimura, N., Cherubini, E., and North, R. A. (1989). Inward rectification in rat nucleus accumbens neurons. J. Neurophysiol. 62, 1280-1286.
78. Wang, W., Zhang, K., Yan, S., Li, A., Hu, X., Zhang, L., and Liu, C. (2011). Enhancement of apamin-sensitive medium afterhyperpolarization current by anandamide and its role in excitability control in cultured hippocampal neurons. Neuropharma-cology 60, 901-909.
79. Williams, J. M., Guevremont, D., Ken-nard, J. T., Mason-Parker, S. E., Tate, W P., and Abraham, W. C. (2003). Long-term regulation of N-methyl-D-aspartate receptor subunits and associated synaptic proteins following hippocampal synaptic plasticity. Neuroscience 118, 1003-1013.
80. Wilson, C.J., and Kawaguchi,Y. (1996). The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J. Neurosci. 16,2397-2410.
81. Zhang, T. A., Hendricson, A. W., and Morrisett, R. A. (2005). Dual synaptic sites of D(1)-dopaminergic regulation of ethanol sensitivity of NMDA receptors in nucleus accumbens. Synapse 58, 30-44.