Ethanol modulation of GABAergic transmission: The view from the slice

Pharmacology and Therapeutics

Volumn 111, Issue 3, 2006, Pages 533-554

  Weiner, J L ^a   Valenzuela, C F ^b  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

Author keywords

Electrophysiology; Ethanol; GABA; Postsynaptic; Presynaptic

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID C RECEPTOR; ALCOHOL; CORTICOTROPIN RELEASING FACTOR; NEUROSTEROID; NEUROTRANSMITTER; PEPTIDE; PROTEIN KINASE;

AMYGDALOID NUCLEUS; BEHAVIOR; BRAIN REGION; BRAIN SLICE; CENTRAL NERVOUS SYSTEM; CEREBELLUM; COGNITION; DEVELOPMENT; ELECTROPHYSIOLOGY; EVOKED RESPONSE; EXPOSURE; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; HIPPOCAMPUS; HUMAN; MAMMAL; NEUROMODULATION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; REVIEW; SYNAPSE;

AMYGDALA; ANIMALS; ETHANOL; GABA MODULATORS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; HUMANS; RECEPTORS, GABA-A; RECEPTORS, GABA-B; SYNAPTIC TRANSMISSION;

EID: 33746734941     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2005.11.002     Document Type: Review

References (184)

1. Aguado F., Carmona M.A., Pozas E., Aguilo A., Martinez-Guijarro F.J., Alcantara S., et al. BDNF regulates spontaneous correlated activity at early developmental stages by increasing synaptogenesis and expression of the K(+)/Cl(-) co-transporter KCC2. Development 130 (2003) 1267-1280
2. - current in mouse hippocampal and cortical neurons. Eur J Pharmacol 187 (1990) 127-130
3. Aguayo L.G., Peoples R.W., Yeh H.H., and Yevenes G.E. GABA(A) receptors as molecular sites of ethanol action. Direct or indirect actions?. Curr Top Med Chem 2 (2002) 869-885
4. Ariwodola O.J., and Weiner J.L. Ethanol potentiation of GABAergic synaptic transmission may be self-limiting: role of presynaptic GABAB receptors. J Neurosci 24 (2004) 10679-10686
5. Ariwodola O.J., Crowder T.L., Grant K.A., Daunais J.B., Friedman D.P., and Weiner J.L. Ethanol modulation of excitatory and inhibitory synaptic transmission in rat and monkey dentate granule neurons. Alcohol Clin Exp Res (2003) 27
6. Ator N.A., Grant K.A., Purdy R.H., Paul S.M., and Griffiths R.R. Drug discrimination analysis of endogenous neuroactive steroids in rats. Eur J Pharmacol 241 (1993) 237-243
7. Barbaccia M.L., Affricano D., Trabucchi M., Purdy R.H., Colombo G., Agabio R., et al. Ethanol markedly increases "GABAergic" neurosteroids in alcohol-preferring rats. Eur J Pharmacol 384 (1999) R1-R2
8. Barry H. Distinctive discriminative effects of ethanol. NIDA Res Monogr (1991) 131-144
9. Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3 (2002) 728-739
10. Berman R.F., and Hannigan J.H. Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy. Hippocampus 10 (2000) 94-110
11. Bloom F.E., and Iversen L.L. Localizing 3H-GABA in nerve terminals of rat cerebral cortex by electron microscopic autoradiography. Nature 229 (1971) 628-630
12. Boehm II S.L., Ponomarev I., Jennings A.W., Whiting P.J., Rosahl T.W., Garrett E.M., et al. γ-Aminobutyric acid A receptor subunit mutant mice: new perspectives on alcohol actions. Biochem Pharmacol 68 (2004) 1581-1602
13. Bonthius D.J., Woodhouse J., Bonthius N.E., Taggard D.A., and Lothman E.W. Reduced seizure threshold and hippocampal cell loss in rats exposed to alcohol during the brain growth spurt. Alcohol Clin Exp Res 25 (2001) 70-82
14. Bonthius D.J., Pantazis N.J., Karacay B., Bonthius N.E., Taggard Da., and Lothman E.W. Alcohol exposure during the brain growth spurt promotes hippocampal seizures, rapid kindling, and spreading depression. Alcohol Clin Exp Res 25 (2001) 734-745
15. Borghese, C. M., Storustovu, S. I., Ebert, B., Herd, M. B., Belelli, D., Lambert, J. J., et al. (in press). The delta subunit of {γ}-aminobutyric acid type A receptors does not confer sensitivity to low concentrations of ethanol. J Pharmacol Exp Ther (Epub ahead of print).
16. Bormann J. The 'ABC' of GABA receptors. Trends Pharmacol Sci 21 (2000) 16-19
17. Bowery N.G., and Enna S.J. γ-Aminobutyric acid(B) receptors: first of the functional metabotropic heterodimers. (erratum appears in J Pharmacol Exp Ther 2000 Apr;293(1):following 312). J Pharmacol Exp Ther 292 (2000) 2-7
18. Cagetti E., Liang J., Spigelman I., and Olsen R.W. 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 (2003) 53-64
19. Carlen P.L., Gurevich N., and Durand D. Ethanol in low doses augments calcium-mediated mechanisms measured intracellularly in hippocampal neurons. Science 215 (1982) 306-309
20. Carr L.G., Spence J.P., Peter Eriksson C.J., Lumeng L., and Li T.K. AA and ANA rats exhibit the R100Q mutation in the GABAA receptor alpha 6 subunit. Alcohol 31 (2003) 93-97
21. Carta M., Ariwodola O.J., Weiner J.L., and Valenzuela C.F. Alcohol potently inhibits the kainate receptor-dependent excitatory drive of hippocampal interneurons. Proc Natl Acad Sci U S A 100 (2003) 6813-6818
22. Carta M., Mameli M., and Valenzuela C.F. Alcohol enhances GABAergic transmission to cerebellar granule cells via an increase in Golgi cell excitability. J Neurosci 24 (2004) 3746-3751
23. Chandler L.J., Harris R.A., and Crews F.T. Ethanol tolerance and synaptic plasticity. Trends Pharmacol Sci 19 (1998) 491-495
24. Cheng G., Gao B., Verbny Y., and Ziskind-Conhaim L. Ethanol reduces neuronal excitability and excitatory synaptic transmission in the developing rat spinal cord. Brain Res 845 (1999) 224-231
25. Cherubini E., and Conti F. Generating diversity at GABAergic synapses. Trends Neurosci 24 (2001) 155-162
26. Chung I., Zhang Y., Eubanks J.H., and Zhang L. Attenuation of hypoxic current by intracellular applications of ATP regenerating agents in hippocampal CA1 neurons of rat brain slices. Neuroscience 86 (1998) 1101-1107
27. Colin-Le Brun I., Ferrand N., Caillard O., Tosetti P., Ben-Ari Y., and Gaiarsa J.L. Spontaneous synaptic activity is required for the formation of functional GABAergic synapses in the developing rat hippocampus. J Physiol 559 (2004) 129-139
28. Colombo G., Addolorato G., Agabio R., Carai M.A., Pibiri F., Serra S., et al. Role of GABA(B) receptor in alcohol dependence: reducing effect of baclofen on alcohol intake and alcohol motivational properties in rats and amelioration of alcohol withdrawal syndrome and alcohol craving in human alcoholics. Neurotox Res 6 (2004) 403-414
29. Couve A., Moss S.J., and Pangalos M.N. GABAB receptors: a new paradigm in G protein signaling. Mol Cell Neurosci 16 (2000) 296-312
30. Criswell H.E., and Breese G.R. A conceptualization of integrated actions of ethanol contributing to its GABAmimetic profile: A commentary. Neuropsychopharmacology 30 (2005) 1407-1425
31. Crowder, T. L., & Weiner, J. L. (2002). Ethanol inhibits presynaptic kainate receptor function at GABAergic synapses in the rat nucleus accumbens core. Program No. 5417 Abstract Viewer Itinerary Planner Washington DC: Society for Neuroscience Online.
32. Crowder T.L., Ariwodola O.J., and Weiner J.L. Ethanol antagonizes kainate receptor-mediated inhibition of evoked GABA(A) inhibitory postsynaptic currents in the rat hippocampal CA1 region. J Pharmacol Exp Ther 303 (2002) 937-944
33. Culmsee C., Bondada S., and Mattson M.P. Hippocampal neurons of mice deficient in DNA-dependent protein kinase exhibit increased vulnerability to DNA damage, oxidative stress and excitotoxicity. Brain Res Mol Brain Res 87 (2001) 257-262
34. Davidoff R.A. Alcohol and presynaptic inhibition in an isolated spinal cord preparation. Arch Neurol 28 (1973) 60-63
35. Deitrich R.A., Dunwiddie T.V., Harris R.A., and Erwin V.G. Mechanism of action of ethanol: initial central nervous system actions. Pharmacol Rev 41 (1989) 489-537
36. Delaney A.J., and Sah P. GABA receptors inhibited by benzodiazepines mediate fast inhibitory synaptic transmission in the central amygdala. J Neurosci 19 (1999) 9698-9704
37. Delaney A.J., and Sah P. Pathway-specific targeting of GABA(A) receptor subtypes to somatic and dendritic synapses in the central amygdala. J Neurophys 86 (2001) 717-723
38. Durand D., Corrigall W.A., Kujtan P., and Carlen P.L. Effect of low concentrations of ethanol on CA1 hippocampal neurons in vitro. Can J Physiol Pharm 59 (1981) 979-984
39. Eggers E.D., O'Brien J.A., and Berger A.J. Developmental changes in the modulation of synaptic glycine receptors by ethanol. J Neurophysiol 84 (2000) 2409-2416
40. Enz R., Brandstatter J.H., Hartveit E., Wassle H., and Bormann J. Expression of GABA receptor rho 1 and rho 2 subunits in the retina and brain of the rat. Eur J Neurosci 7 (1995) 1495-1501
41. Eriksson C.J., and Sarviharju M. Motor impairment, narcosis and hypothermia by ethanol: separate genetic mechanisms. Alcohol 1 (1984) 59-62
42. Farrant M., and Nusser Z. Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6 (2005) 215-229
43. Freund R.K., and Palmer M.R. 8-Bromo-cAMP mimics beta-adrenergic sensitization of GABA responses to ethanol in cerebellar Purkinje neurons in vivo. Alcohol Clin Exp Res 20 (1996) 408-412
44. Freund R.K., and Palmer M.R. Beta adrenergic sensitization of γ-aminobutyric acid receptors to ethanol involves a cyclic AMP/protein kinase A second-messenger mechanism. J Pharmacol Exp Ther 280 (1997) 1192-1200
45. Frye G.D., and Breese G.R. GABAergic modulation of ethanol-induced motor impairment. J Pharmacol Exp Ther 223 (1982) 750-756
46. Frye G.D., and Fincher A. Sensitivity of postsynaptic GABAB receptors on hippocampal CA1 and CA3 pyramidal neurons to ethanol. Brain Res 735 (1996) 239-248
47. Gaiarsa J.L., McLean H., Congar P., Leinekugel X., Khazipov R., Tseeb V., et al. Postnatal maturation of γ-aminobutyric acidA and B-mediated inhibition in the CA3 hippocampal region of the rat. J Neurobiol 26 (1995) 339-349
48. Galindo R., Zamudio P., and Valenzuela C. Alcohol is a potent stimulant of immature neuronal networks: implications for fetal alcohol spectrum disorder. J Neurochem 94 (2005) 1500-1511
49. Grobin A.C., Matthews D.B., Devaud L.L., and Morrow A.L. The role of GABA(A) receptors in the acute and chronic effects of ethanol. Psychopharmacologia 139 (1998) 2-19
50. Grobin A.C., Fritschy J.M., and Morrow A.L. Chronic ethanol administration alters immunoreactivity for GABA(A) receptor subunits in rat cortex in a region-specific manner. Alcohol Clin Exp Res 24 (2000) 1137-1144
51. Grobin A.C., Papadeas S.T., and Morrow A.L. Regional variations in the effects of chronic ethanol administration on GABA(A) receptor expression: potential mechanisms. Neurochem Int 37 (2000) 453-461
52. Hakkinen H.M., and Kulonen E. Ethanol intoxication and γ-aminobutyric acid. J Neurochem 27 (1976) 631-633
53. Hamann M., Rossi D.J., and Attwell D. Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33 (2002) 625-633
54. Hamilton D.A., Kodituwakku P., Sutherland R.J., and Savage D.D. Children with fetal alcohol syndrome are impaired at place learning but not cued-navigation in a virtual Morris water task. Behav Brain Res 143 (2003) 85-94
55. Hanchar H.J., Dodson P.D., Olsen R.W., Otis T.S., and Wallner M. Alcohol-induced motor impairment caused by increased extrasynaptic GABA(A) receptor activity. Nat Neurosci 8 (2005) 339-345
56. Harris R.A., McQuilkin S.J., Paylor R., Abeliovich A., Tonegawa S., and Wehner J.M. Mutant mice lacking the gamma isoform of protein kinase C show decreased behavioral actions of ethanol and altered function of γ-aminobutyrate type A receptors. (see comments). Proc Natl Acad Sci U S A 92 (1995) 3658-3662
57. Hartley T., and Burgess N. Complementary memory systems: competition, cooperation and compensation. Trends Neurosci 28 (2005) 169-170
58. 2+-supported, asynchronous NMDAR mEPSCs in rat hippocampal slices. J Neurophysiol 91 (2004) 2568-2577
59. Hevers W., and Luddens H. The diversity of GABAA receptors. Pharmacological and electrophysiological properties of GABAA channel subtypes. Mol Neurobiol 18 (1998) 35-86
60. Hodge C.W., and Alken A.S. Discriminative stimulus function of ethanol: role of GABAA receptors in the nucleus accumbens. Alcohol Clin Exp Res 20 (1996) 1221-1228
61. Hubner C.A., Stein V., Hermans-Borgmeyer I., Meyer T., Ballanyi K., and Jentsch T.J. Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30 (2001) 515-524
62. Jones K.A., Borowsky B., Tamm J.A., Craig D.A., Durkin M.M., Dai M., et al. GABA(B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2. Nature 396 (1998) 674-679
63. Kajikawa Y., Saitoh N., and Takahashi T. GTP-binding protein beta gamma subunits mediate presynaptic calcium current inhibition by GABA(B) receptor. Proc Natl Acad Sci U S A 98 (2001) 8054-8058
64. Kaneda M., Farrant M., and Cull-Candy S.G. Whole-cell and single-channel currents activated by GABA and glycine in granule cells of the rat cerebellum. J Physiol 485 Pt 2 (1995) 419-435
65. Kang M., Spigelman I., Sapp D.W., and Olsen R.W. Persistent reduction of GABA(A) receptor-mediated inhibition in rat hippocampus after chronic intermittent ethanol treatment. Brain Res 709 (1996) 221-228
66. Kang J., Jiang L., Goldman S.A., and Nedergaard M. Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1 (1998) 683-692
67. Kang M.H., Spigelman I., and Olsen R.W. Alteration in the sensitivity of GABA(A) receptors to allosteric modulatory drugs in rat hippocampus after chronic intermittent ethanol treatment. Alcohol Clin Exp Res 22 (1998) 2165-2173
68. Kasyanov A.M., Safiulina V.F., Voronin L.L., and Cherubini E. From The Cover: GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus. Proc Natl Acad Sci U S A 101 (2004) 3967-3972
69. Kaupmann K., Malitschek B., Schuler V., Heid J., Froestl W., Beck P., et al. GABA(B)-receptor subtypes assemble into functional heteromeric complexes. Nature 396 (1998) 683-687
70. Klein R.L., and Harris R.A. Regulation of GABAA receptor structure and function by chronic drug treatments in vivo and with stably transfected cells. Jpn J Pharmacol 70 (1996) 1-15
71. Kliethermes C.L. Anxiety-like behaviors following chronic ethanol exposure. Neurosci Biobehav Rev 28 (2005) 837-850
72. Kline F.S., and Young A.M. Differential modification of pentobarbital stimulus control by d-amphetamine and ethanol. Pharmacol Biochem Behav 24 (1986) 1305-1313
73. Kokka N., Sapp D.W., Taylor A.M., and Olsen R.W. The kindling model of alcohol dependence: similar persistent reduction in seizure threshold to pentylenetetrazol in animals receiving chronic ethanol or chronic pentylenetetrazol. Alcohol Clin Exp Res 17 (1993) 525-531
74. Korpi E.R., Kleingoor C., Kettenmann H., and Seeburg P.H. Benzodiazepine-induced motor impairment linked to point mutation in cerebellar GABAA receptor. Nature 361 (1993) 356-359
75. Krnjevic K. Role of GABA in cerebral cortex. Can J Physiol Pharm 75 (1997) 439-451
76. Kumar S., Fleming R.L., and Morrow A.L. Ethanol regulation of γ-aminobutyric acid A receptors: genomic and nongenomic mechanisms. Pharmacol Ther 101 (2004) 211-226
77. Lambert J.J., Belelli D., Harney S.C., Peters J.A., and Frenguelli B.G. Modulation of native and recombinant GABA(A) receptors by endogenous and synthetic neuroactive steroids. Brain Res Brain Res Rev 37 (2001) 68-80
78. Lauri S.E., Lamsa K., Pavlov I., Riekki R., Johnson B.E., Molnar E., et al. Activity blockade increases the number of functional synapses in the hippocampus of newborn rats. Mol Cell Neurosci 22 (2003) 107-117
79. Le A.D., Khanna J.M., Kalant H., and Grossi F. Tolerance to and cross-tolerance among ethanol, pentobarbital and chlordiazepoxide. Pharmacol Biochem Behav 24 (1986) 93-98
80. 2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus. Neuron 18 (1997) 243-255
81. - concentrations depress G-protein-modulated ionic conductances. J Neurosci 17 (1997) 6133-6141
82. Li Q., Wilson W.A., and Swartzwelder H.S. Developmental differences in the sensitivity of hippocampal GABAA receptor-mediated IPSCS to ethanol. Alcohol Clin Exp Res 27 (2003) 2017-2022
83. Li Q., Wilson W.A., and Swartzwelder H.S. Developmental differences in the sensitivity of GABA-A receptor mediated sIPSCs and mIPSCs to ethanol. Alcohol Clin Exp Res 29 (2005) 94A (Suppl)
84. Liang J., Cagetti E., Olsen R.W., and Spigelman I. Altered pharmacology of synaptic and extrasynaptic GABAA receptors on CA1 hippocampal neurons is consistent with subunit changes in a model of alcohol withdrawal and dependence. J Pharmacol Exp Ther 310 (2004) 1234-1245
85. Liljequist S., and Engel J. Effects of GABAergic agonists and antagonists on various ethanol-induced behavioral changes. Psychopharmacology 78 (1982) 71-75
86. Lin A.M., Freund R.K., and Palmer M.R. Ethanol potentiation of GABA-induced electrophysiological responses in cerebellum: requirement for catecholamine modulation. Neurosci Lett 122 (1991) 154-158
87. Lin A.M., Freund R.K., Hoffer B.J., and Palmer M.R. Ethanol-induced depressions of cerebellar Purkinje neurons are potentiated by beta-adrenergic mechanisms in rat brain. J Pharmacol Exp Ther 271 (1994) 1175-1180
88. Littleton J. Neurochemical mechanisms underlying alcohol withdrawal. Alcohol Health Res World 22 (1998) 13-24
89. Macdonald R.L. Ethanol, γ-aminobutyrate type A receptors, and protein kinase C phosphorylation. (comment). Proc Natl Acad Sci U S A 92 (1995) 3633-3635
90. Macdonald R.L., and Olsen R.W. GABAA receptor channels. Annu Rev Neurosci 17 (1994) 569-602
91. Mameli, M., Carta, M., & Valenzuela, C. F. (2005a). Effect of ethanol on GABAergic transmission in cerebellar Purkinje neurons. SFN Meeting Abstract.
92. Mameli M., Zamudio P.A., Carta M., and Valenzuela C.F. Developmentally regulated actions of alcohol on hippocampal glutamatergic transmission. J Neurosci 25 (2005) 8027-8036
93. Margeta-Mitrovic M., Mitrovic I., Riley R.C., Jan L.Y., and Basbaum A.I. Immunohistochemical localization of GABA(B) receptors in the rat central nervous system. J Comp Neurol 405 (1999) 299-321
94. Marshall F.H., Jones K.A., Kaupmann K., and Bettler B. GABAB receptors-the first 7TM heterodimers. Trends Pharmacol Sci 20 (1999) 396-399
95. Martina M., Strata F., and Cherubini E. Whole cell and single channel properties of a new GABA receptor transiently expressed in the Hippocampus. J Neurophysiol 73 (1995) 902-906
96. Martz A., Deitrich R.A., and Harris R.A. Behavioral evidence for the involvement of γ-aminobutyric acid in the actions of ethanol. Eur J Pharmacol 89 (1983) 53-62
97. McKernan R.M., and Whiting P.J. Which GABAA-receptor subtypes really occur in the brain?. (see comments). Trends Neurosci 19 (1996) 139-143
98. Melis M., Camarini R., Ungless M.A., and Bonci A. Long-lasting potentiation of GABAergic synapses in dopamine neurons after a single in vivo ethanol exposure. J Neurosci 22 (2002) 2074-2082
99. Mihic S.J. Acute effects of ethanol on GABAA and glycine receptor function. Neurochem Int 35 (1999) 115-123
100. Mihic S.J., Wu P.H., and Kalant H. Differences among effects of sedative-hypnotic drugs on GABA-mediated chloride flux: quench flow studies. Brain Res 555 (1991) 259-264
101. Mihic S.J., Kalant H., Liu J.F., and Wu P.H. Role of the γ-aminobutyric acid receptor/chloride channel complex in tolerance to ethanol and cross-tolerance to diazepam and pentobarbital. J Pharmacol Exp Ther 261 (1992) 108-113
102. Mihic S.J., Ye Q., Wick M.J., Koltchine V.V., Krasowski M.D., Finn S.E., et al. Sites of alcohol and volatile anaesthetic action on GABA(A) and glycine receptors. (see comments). Nature 389 (1997) 385-389
103. Misgeld U., Bijak M., and Jarolimek W. A physiological role for GABAB receptors and the effects of baclofen in the mammalian central nervous system. Prog Neurobiol 46 (1995) 423-462
104. Moore S.D., Kang-Park M.-H., Kieffer B.L., Roberts A.J., Madamba S.G., and Siggins G.R. Delta opioid receptor role in ethanol reinforcement and amygdalar electrophysiological parameters. Alcohol Clin Exp Res 29 (2005) 181A (Suppl)
105. Morrisett R.A., and Swartzwelder H.S. Attenuation of hippocampal long-term potentiation by ethanol: a patch-clamp analysis of glutamatergic and GABAergic mechanisms. J Neurosci 13 (1993) 2264-2272
106. Morrow A.L., Suzdak P.D., and Paul S.M. Benzodiazepine, barbiturate, ethanol and hypnotic steroid hormone modulation of GABA-mediated chloride ion transport in rat brain synaptoneurosomes. Adv Biochem Psychopharmacol 45 (1988) 247-261
107. Morrow A.L., Janis G.C., VanDoren M.J., Matthews D.B., Samson H.H., Janak P.H., et al. Neurosteroids mediate pharmacological effects of ethanol: a new mechanism of ethanol action?. Alcohol Clin Exp Res 23 (1999) 1933-1940
108. Morrow A.L., VanDoren M.J., Penland S.N., and Matthews D.B. The role of GABAergic neuroactive steroids in ethanol action, tolerance and dependence. Brain Res Brain Res Rev 37 (2001) 98-109
109. Mouginot D., Kombian S.B., and Pittman Q.J. Activation of presynaptic GABAB receptors inhibits evoked IPSCs in rat magnocellular neurons in vitro. J Neurophysiol 79 (1998) 1508-1517
110. Nestoros J.N. Ethanol selectively potentiates GABA-mediated inhibition of single feline cortical neurons. Life Sci 26 (1980) 519-523
111. Nie Z., Madamba S.G., and Siggins G.R. Ethanol enhances γ-aminobutyric acid responses in a subpopulation of nucleus accumbens neurons: role of metabotropic glutamate receptors. J Pharmacol Exp Ther 293 (2000) 654-661
112. Nie Z., Schweitzer P., Roberts A.J., Madamba S.G., Moore S.D., and Siggins G.R. Ethanol augments GABAergic transmission in the central amygdala via CRF1 receptors. Science 303 (2004) 1512-1514
113. Nishikawa M., Hirouchi M., and Kuriyama K. Functional coupling of Gi subtype with GABAB receptor/adenylyl cyclase system: analysis using a reconstituted system with purified GTP-binding protein from bovine cerebral cortex. Neurochem Int 31 (1997) 21-25
114. Nusser Z., Sieghart W., Benke D., Fritschy J.M., and Somogyi P. Differential synaptic localization of two major γ-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc Natl Acad Sci U S A 93 (1996) 11939-11944
115. Ortells M.O., and Lunt G.G. Evolutionary history of the ligand-gated ion-channel superfamily of receptors. (see comments). Trends Neurosci 18 (1995) 121-127
116. Osmanovic S.S., and Shefner S.A. Enhancement of current induced by superfusion of GABA in locus coeruleus neurons by pentobarbital, but not ethanol. Brain Res 517 (1990) 324-329
117. Pearce R.A. Physiological evidence for two distinct GABAA responses in rat hippocampus. Neuron 10 (1993) 189-200
118. Pearce R.A., Grunder S.D., and Faucher L.D. Different mechanisms for use-dependent depression of two GABAA-mediated IPSCs in rat hippocampus. J Physiol 484 (1995) 425-435
119. Pierucci-Lagha A., Covault J., Feinn R., Nellissery M., Hernandez-Avila C., Oncken C., et al. GABRA2 alleles moderate the subjective effects of alcohol, which are attenuated by finasteride. Neuropsychopharmacology 30 (2005) 1193-1203
120. Poelchen W., Proctor W.R., and Dunwiddie T.V. The in vitro ethanol sensitivity of hippocampal synaptic γ-aminobutyric acid(A) responses differs in lines of mice and rats genetically selected for behavioral sensitivity or insensitivity to ethanol. J Pharmacol Exp Ther 295 (2000) 741-746
121. Poisbeau P., Feltz P., and Schlichter R. Modulation of GABAA receptor-mediated IPSCs by neuroactive steroids in a rat hypothalamo-hypophyseal coculture model. J Physiol 500 Pt 2 (1997) 475-485
122. Poltl A., Hauer B., Fuchs K., Tretter V., and Sieghart W. Subunit composition and quantitative importance of GABAA receptor subtypes in the cerebellum of mouse and rat. J Neurochem 87 (2003) 1444-1455
123. Proctor W.R., Allan A.M., and Dunwiddie T.V. Brain region-dependent sensitivity of GABAA receptor-mediated responses to modulation by ethanol. Alcohol Clin Exp Res 16 (1992) 480-489
124. Proctor W.R., Poelchen W., Bowers B.J., Wehner J.M., Messing R.O., and Dunwiddie T.V. Ethanol differentially enhances hippocampal GABA A receptor-mediated responses in protein kinase C gamma (PKC gamma) and PKC epsilon null mice. J Pharmacol Exp Ther 305 (2003) 264-270
125. Prosser H.M., Gill C.H., Hirst W.D., Grau E., Robbins M., Calver A., et al. Epileptogenesis and enhanced prepulse inhibition in GABA(B1)-deficient mice. Mol Cell Neurosci 17 (2001) 1059-1070
126. Qian H., and Dowling J.E. Novel GABA responses from rod-driven retinal horizontal cells. Nature 361 (1993) 162-164
127. Radcliffe R.A., Hoffmann S.E., Deng X.S., Asperi W., Fay T., Bludeau P., et al. Behavioral characterization of alcohol-tolerant and alcohol-nontolerant rat lines and an f(2) generation. Behav Genet 34 (2004) 453-463
128. Reynolds J.N., and Prasad A. Ethanol enhances GABAA receptor-activated chloride currents in chick cerebral cortical neurons. Brain Res 564 (1991) 138-142
129. Reynolds J.N., Prasad A., and MacDonald J.F. Ethanol modulation of GABA receptor-activated Cl-currents in neurons of the chick, rat and mouse central nervous system. Eur J Pharmacol 224 (1992) 173-181
130. Roberto M., Madamba S.G., Moore S.D., Tallent M.K., and Siggins G.R. Ethanol increases GABAergic transmission at both pre- and postsynaptic sites in rat central amygdala neurons. Proc Natl Acad Sci U S A 100 (2003) 2053-2058
131. Roberto M., Madamba S.G., Stouffer D.G., Parsons L.H., and Siggins G.R. Increased GABA release in the central amygdala of ethanol-dependent rats. J Neurosci 24 (2004) 10159-10166
132. Roberto M., Schweitzer P., Madamba S., Nie Z., and Siggins G. Ethanol-CRF interactions at GABAergic synapses in the rat central amygdala. Alcohol Clin Exp Res 29 (2005) 11A (Suppl)
133. Robinson D.W., and Cameron W.E. Time-dependent changes in input resistance of rat hypoglossal motoneurons associated with whole-cell recording. J Neurophysiol 83 (2000) 3160-3164
134. Rudolph U., and Mohler H. Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu Rev Pharmacol Toxicol 44 (2004) 475-498
135. Saba L., Porcella A., Congeddu E., Colombo G., Peis M., Pistis M., et al. The R100Q mutation of the GABA(A) alpha(6) receptor subunit may contribute to voluntary aversion to ethanol in the sNP rat line. Brain Res Mol Brain Res 87 (2001) 263-270
136. Sanna E., Talani G., Busonero F., Pisu M.G., Purdy R.H., Serra M., et al. Brain steroidogenesis mediates ethanol modulation of GABAA receptor activity in rat hippocampus. J Neurosci 24 (2004) 6521-6530
137. Schuckit M.A. Low level of response to alcohol as a predictor of future alcoholism. Am J Psychiatr 151 (1994) 184-189
138. Schuckit M.A., and Smith T.L. An 8-year follow-up of 450 sons of alcoholic and control subjects. Arch Gen Psychiatry 53 (1996) 202-210
139. Schuler V., Luscher C., Blanchet C., Klix N., Sansig G., Klebs K., et al. Epilepsy, hyperalgesia, impaired memory, and loss of pre- and postsynaptic GABA(B) responses in mice lacking GABA(B(1)). Neuron 31 (2001) 47-58
140. Schummers J., and Browning M.D. Evidence for a role for GABA(A) and NMDA receptors in ethanol inhibition of long-term potentiation. Brain Res Mol Brain Res 94 (2001) 9-14
141. Sebe J.Y., Eggers E.D., and Berger A.J. Differential effects of ethanol on GABA(A) and glycine receptor-mediated synaptic currents in brain stem motoneurons. J Neurophysiol 90 (2003) 870-875
142. Sieghart W. Structure and pharmacology of γ-aminobutyric acidA receptor subtypes. Pharmacol Rev 47 (1995) 181-234
143. Siggins G.R., Nie Z., and Madamba S.G. A metabotropic hypothesis for ethanol sensitivity of GABAergic and glutamatergic central synapses. In: Liu Y., and Hunt W.A. (Eds). The Drunken Synapse (1999), Plenum, New York 135-143
144. Siggins G.R., Pittman Q.J., and French E.D. Effects of ethanol on CA1 and CA3 pyramidal cells in the hippocampal slice preparation: an intracellular study. Brain Res 414 (1987) 22-34
145. Siggins G.R., Roberto M., and Nie Z. The tipsy terminal: presynaptic effects of ethanol. Pharmacol Ther 107 (2005) 80-98
146. Signore A.P., and Yeh H.H. Chronic exposure to ethanol alters GABA(A) receptor-mediated responses of layer II pyramidal cells in adult rat piriform cortex. J Neurophysiol 84 (2000) 247-254
147. Sipila S.T., Huttu K., Soltesz I., Voipio J., and Kaila K. Depolarizing GABA acts on intrinsically bursting pyramidal neurons to drive giant depolarizing potentials in the immature hippocampus. J Neurosci 25 (2005) 5280-5289
148. Sloviter R.S., Ali-Akbarian L., Elliott R.C., Bowery B.J., and Bowery N.G. Localization of GABA(B) (R1) receptors in the rat hippocampus by immunocytochemistry and high resolution autoradiography, with specific reference to its localization in identified hippocampal interneuron subpopulations. Neuropharmacology 38 (1999) 1707-1721
149. Soldo B.L., Proctor W.R., and Dunwiddie T.V. Ethanol differentially modulates GABAA receptor-mediated chloride currents in hippocampal, cortical, and septal neurons in rat brain slices. Synapse 18 (1994) 94-103
150. Soldo B.L., Proctor W.R., and Dunwiddie T.V. Ethanol selectively enhances the hyperpolarizing component of neocortical neuronal responses to locally applied GABA. Brain Res 800 (1998) 187-197
151. Spigelman I., Liang J., Cagetti E., and Olsen R. Anxiolytic and sedative actions of ethanolrelated to enhancement of GABAA reeceptor-mediated synaptic and extrasynaptic currents in hippocampal neurons from chronic intermittend ethanol-treated rats. Alcohol Clin Exp Res 28 (2004) 92A (Suppl)
152. Staley K.J., Soldo B.L., and Proctor W.R. Ionic mechanisms of neuronal excitation by inhibitory GABAA receptors. Science 269 (1995) 977-981
153. Steffensen S.C., Nie Z., Criado J.R., and Siggins G.R. Ethanol inhibition of N-methyl-d-aspartate responses involves presynaptic γ-aminobutyric acid(B) receptors. J Pharmacol Exp Ther 294 (2000) 637-647
154. Sundstrom-Poromaa I., Smith D.H., Gong Q.H., Sabado T.N., Li X., Light A., et al. Hormonally regulated alpha(4)beta(2)delta GABA(A) receptors are a target for alcohol. Nat Neurosci 5 (2002) 721-722
155. Suzdak P.D., Schwartz R.D., Skolnick P., and Paul S.M. Ethanol stimulates γ-aminobutyric acid receptor-mediated chloride transport in rat brain synaptoneurosomes. Proc Natl Acad Sci U S A 83 (1986) 4071-4075
156. Suzdak P.D., Glowa J.R., Crawley J.N., Schwartz R.D., Skolnick P., and Paul S.M. A selective imidazobenzodiazepine antagonist of ethanol in the rat. Science 234 (1986) 1243-1247
157. Thompson S.M. Modulation of inhibitory synaptic transmission in the hippocampus. Prog Neurobiol 42 (1994) 575-609
158. Tremblay E., Ben-Ari Y., and Roisin M.P. Different GABAB-mediated effects on protein kinase C activity and immunoreactivity in neonatal and adult rat hippocampal slices. J Neurochem 65 (1995) 863-870
159. Vale C., and Sanes D.H. Afferent regulation of inhibitory synaptic transmission in the developing auditory midbrain. J Neurosci 20 (2000) 1912-1921
160. Valenzuela C.F., Mameli M., and Carta M. Single-amino-acid difference in the sequence of alpha6 subunit dramatically increases the ethanol sensitivity of recombinant GABAA receptors. Alcohol Clin Exp Res 29 (2005) 1356-1357
161. VanDoren M.J., Matthews D.B., Janis G.C., Grobin A.C., Devaud L.L., and Morrow A.L. Neuroactive steroid 3alpha-hydroxy-5alpha-pregnan-20-one modulates electrophysiological and behavioral actions of ethanol. J Neurosci 20 (2000) 1982-1989
162. Vargas G., Yeh T.Y., Blumenthal D.K., and Lucero M.T. Common components of patch-clamp internal recording solutions can significantly affect protein kinase A activity. Brain Res 828 (1999) 169-173
163. Velumian A.A., Zhang L., Pennefather P., and Carlen P.L. Reversible inhibition of IK, IAHP, Ih and ICa currents by internally applied gluconate in rat hippocampal pyramidal neurones. Pflugers Arch 433 (1997) 343-350
164. Vivian J.A., Green H.L., Young J.E., Majerksy L.S., Thomas B.W., Shively C.A., et al. Induction and maintenance of ethanol self-administration in cynomolgus monkeys (Macaca fascicularis): long-term characterization of sex and individual differences. Alcohol Clin Exp Res 25 (2001) 1087-1097
165. Wall M.J., and Usowicz M.M. Development of action potential-dependent and independent spontaneous GABAA receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur J Neurosci 9 (1997) 533-548
166. Wallner M., Hanchar H.J., and Olsen R.W. Ethanol enhances alpha 4 beta 3 delta and alpha 6 beta 3 delta γ-aminobutyric acid type A receptors at low concentrations known to affect humans. Proc Natl Acad Sci U S A 100 (2003) 15218-15223
167. Wan F.J., Berton F., Madamba S.G., Francesconi W., and Siggins G.R. Low ethanol concentrations enhance GABAergic inhibitory postsynaptic potentials in hippocampal pyramidal neurons only after block of GABAB receptors. Proc Natl Acad Sci U S A 93 (1996) 5049-5054
168. Watson P.L., Weiner J.L., and Carlen P.L. Effects of variations in hippocampal slice preparation protocol on the electrophysiological stability, epileptogenicity and graded hypoxia responses of CA1 neurons. Brain Res 775 (1997) 134-143
169. Wei W., Faria L.C., and Mody I. Low ethanol concentrations selectively augment the tonic inhibition mediated by delta subunit-containing GABAA receptors in hippocampal neurons. J Neurosci 24 (2004) 8379-8382
170. Weiner J.L. Electrophysiological assessment of synaptic transmission in
171. Weiner J.L., Zhang L., and Carlen P.L. Potentiation of GABAA-mediated synaptic current by ethanol in hippocampal CA1 neurons: possible role of protein kinase C. J Pharmacol Exp Ther 268 (1994) 1388-1395
172. Weiner J.L., Gu C., and Dunwiddie T.V. Differential ethanol sensitivity of subpopulations of GABAA synapses onto rat hippocampal CA1 pyramidal neurons. J Neurophysiol 77 (1997) 1306-1312
173. Weiner J.L., Valenzuela C.F., Watson P.L., Frazier C.J., and Dunwiddie T.V. Elevation of basal protein kinase C activity increases ethanol sensitivity of GABA(A) receptors in rat hippocampal CA1 pyramidal neurons. J Neurochem 68 (1997) 1949-1959
174. Weiner J.L., Ariwodola O.J., Bates W.H., Bryant V., Silberman Y., Daunais J.B., et al. Presynaptic mechanisms underlying ethanol actions at GABAergic synapses in rat and monkey hippocampus. Alcohol Clin Exp Res 29 (2005) 187A (Suppl)
175. Werner D.F., Blednov Y.A., Ferguson C., Weiner J.L., Matthews D.B., Harris R.A., et al. Ethanol responses of GABAA receptor alpha1 subunit knockin mice. Program No. 84414 Abstract Viewer Itinerary Planner (2004), Society for Neuroscience Online, Washington, DC (online)
176. White G., Lovinger D.M., and Weight F.F. Ethanol inhibits NMDA-activated current but does not alter GABA-activated current in an isolated adult mammalian neuron. Brain Res 507 (1990) 332-336
177. White J.H., Wise A., Main M.J., Green A., Fraser N.J., Disney G.H., et al. Heterodimerization is required for the formation of a functional GABA(B) receptor. (see comments). Nature 396 (1998) 679-682
178. Wisden W., Korpi E.R., and Bahn S. The cerebellum: a model system for studying GABAA receptor diversity. Neuropharmacology 35 (1996) 1139-1160
179. Wu P.H., Poelchen W., and Proctor W.R. Differential GABAB receptor modulation of ethanol effects on GABA(A) synaptic activity in hippocampal CA1 neurons. J Pharmacol Exp Ther 312 (2005) 1082-1089
180. Yeh H.H., Grigorenko E.V., and Veruki M.L. Correlation between a bicuculline-resistant response to GABA and GABAA receptor rho 1 subunit expression in single rat retinal bipolar cells. Vis Neurosci 13 (1996) 283-292
181. Zhan R.Z., Nadler J.V., and Schwartz-Bloom R.D. Depressed responses to applied and synaptically-released GABA in CA1 pyramidal cells, but not in CA1 interneurons, after transient forebrain ischemia. J Cereb Blood Flow Metab (2005) 1-15 (advance online publication, 15 Jun)
182. Zhang L., Weiner J.L., Valiante T.A., Velumian A.A., Watson P.L., Jahromi S.S., et al. Whole-cell recording of the Ca(2+)-dependent slow afterhyperpolarization in hippocampal neurones: effects of internally applied anions. Pflugers Arch 426 (1994) 247-253
183. Zhu P.J., and Lovinger D.M. Ethanol directly increases GABA release from GABAergic presynaptic terminals in basolateral amygdala. Alcohol Clin Exp Res 29 (2005) 187A (Suppl)
184. Ziskind-Conhaim L., Gao B.X., and Hinckley C. Ethanol dual modulatory actions on spontaneous postsynaptic currents in spinal motoneurons. J Neurophysiol 89 (2003) 806-813