Synaptic targets: chronic alcohol actions
Open accessAbstract
Alcohol acts on numerous cellular and molecular targets to regulate neuronal communication within the brain. Chronic alcohol exposure and acute withdrawal generate prominent neuroadaptations at synapses, including compensatory effects on the expression, localization and function of synaptic proteins, channels and receptors. The present article reviews the literature describing the synaptic effects of chronic alcohol exposure and their relevance for synaptic transmission in the central nervous system. This review is not meant to be comprehensive, but rather to highlight the effects that have been observed most consistently and that are thought to contribute to the development of alcohol dependence and the negative aspects of withdrawal. Specifically, we will focus on the major excitatory and inhibitory neurotransmitters in the brain, glutamate and GABA, respectively, and how their neuroadaptations after chronic alcohol exposure contributes to alcohol reinforcement, dependence and withdrawal. This article is part of the Special Issue entitled "Alcoholism".
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- Aguayo LG Peoples RW Yeh HH Yevenes GE GABA(A) receptors as molecular sites of ethanol action. Direct or indirect actions? Curr Top Med Chem 2002 2 869 885 12171577
- Akinshola BE Stewart RR Karvonen LL Taylor RE Liesi P Involvement of non-NMDA receptors in the rescue of weaver cerebellar granule neurons and sensitivity to ethanol of cerebellar AMPA receptors in oocytes Brain Res Mol Brain Res 2001 93 8 17 11532333
- Akinshola BE Yasuda RP Peoples RW Taylor RE Ethanol sensitivity of recombinant homomeric and heteromeric AMPA receptor subunits expressed in Xenopus oocytes Alcohol Clin Exp Res 2003 27 1876 1883 14691374
- Allan AM Harris RA Acute and chronic ethanol treatments alter GABA receptor-operated chloride channels Pharmacol Biochem Behav 1987 27 665 670 2443933
- Anderson NJ Daunais JB Friedman DP Grant KA McCool BA Long-term ethanol self-administration by the nonhuman primate, Macaca fascicularis, decreases the benzodiazepine sensitivity of amygdala GABA(A) receptors Alcohol Clin Exp Res 2007 31 1061 1070 17428292 PMC2288551
- Ariwodola OJ Crowder TL Grant KA Daunais JB Friedman DP Weiner JL Ethanol modulation of excitatory and inhibitory synaptic transmission in rat and monkey dentate granule neurons Alcohol Clin Exp Res 2003 27 1632 1639 14574234
- Ariwodola OJ Weiner JL Ethanol potentiation of GABAergic synaptic transmission may be self-limiting: role of presynaptic GABAB receptors J Neurosci 2004 24 10679 10686 15564584 PMC6730127
- Ary AW Cozzoli DK Finn DA Crabbe JC Dehoff MH Worley PF Szumlinski KK Ethanol up-regulates nucleus accumbens neuronal activity dependent pentraxin (Narp): implications for alcohol-induced behavioral plasticity Alcohol 2012 46 377 387 22444953 PMC3358440
- Baculis BC Diaz MR Valenzuela CF Third trimester-equivalent ethanol exposure increases anxiety-like behavior and glutamatergic transmission in the basolateral amygdala Pharmacol Biochem Behav 2015 137 78 85 26284742 PMC4567916
- Baculis BC Valenzuela CF Ethanol exposure during the third trimester equivalent does not affect GABAA or AMPA receptor-mediated spontaneous synaptic transmission in rat CA3 pyramidal neurons J Negat Results Biomed 2015 14 19 26627643 PMC4667401
- Bjork K Rimondini R Hansson AC Terasmaa A Hyytia P Heilig M Sommer WH Modulation of voluntary ethanol consumption by beta-arrestin 2 Faseb J 2008 22 2552 2560 18367649
- Bliss TV Collingridge GL Morris RG Synaptic plasticity in health and disease: introduction and overview Philos Trans R Soc Lond B Biol Sci 2014 369 20130129 24298133 PMC3843863
- Bohnsack JP Carlson SL Morrow AL Differential regulation of synaptic and extrasynaptic alpha4 GABA(A) receptor populations by protein kinase A and protein kinase C in cultured cortical neurons Neuropharmacology 2016 105 124 132 26767953 PMC4873390
- Botta P Radcliffe RA Carta M Mameli M Daly E Floyd KL Deitrich RA Valenzuela CF Modulation of GABAA receptors in cerebellar granule neurons by ethanol: a review of genetic and electrophysiological studies Alcohol 2007 41 187 199 17521847 PMC1986723
- Boyle AE Segal R Smith BR Amit Z Bidirectional effects of GABAergic agonists and antagonists on maintenance of voluntary ethanol intake in rats Pharmacol Biochem Behav 1993 46 179 182 8255910
- Brandon N Jovanovic J Moss S Multiple roles of protein kinases in the modulation of gamma-aminobutyric acid(A) receptor function and cell surface expression Pharmacol Ther 2002 94 113 122 12191597
- Breese GR Criswell HE Carta M Dodson PD Hanchar HJ Khisti RT Mameli M Ming Z Morrow AL Olsen RW Otis TS Parsons LH Penland SN Roberto M Siggins GR Valenzuela CF Wallner M Basis of the gabamimetic profile of ethanol Alcohol Clin Exp Res 2006 30 731 744 16573592 PMC2958095
- Bruckner MK Rossner S Arendt T Differential changes in the expression of AMPA receptors genes in rat brain after chronic exposure to ethanol: an in situ hybridization study J Hirnforsch 1997 38 369 376 9350508
- Buck KJ Harris RA Benzodiazepine agonist and inverse agonist actions on GABAA receptor-operated chloride channels. II. Chronic effects of ethanol J Pharmacol Exp Ther 1990 253 713 719 2160008
- Cagetti E Liang J Spigelman I Olsen RW 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 2003 63 53 64 12488536
- Cardoso RA Brozowski SJ Chavez-Noriega LE Harpold M Valenzuela CF Harris RA Effects of ethanol on recombinant human neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes J Pharmacol Exp Ther 1999 289 774 780 10215652
- Carlson SL Bohnsack JP Morrow AL Ethanol Regulation of Synaptic GABAA alpha4 Receptors Is Prevented by Protein Kinase A Activation J Pharmacol Exp Ther 2016a 357 10 16 26857960 PMC4809316
- Carlson SL Bohnsack JP Patel V Morrow AL Regulation of Extrasynaptic GABAA alpha4 Receptors by Ethanol-Induced Protein Kinase A, but Not Protein Kinase C Activation in Cultured Rat Cerebral Cortical Neurons J Pharmacol Exp Ther 2016b 356 148 156 26483396 PMC4702069
- Carpenter-Hyland EP Woodward JJ Chandler LJ Chronic ethanol induces synaptic but not extrasynaptic targeting of NMDA receptors J Neurosci 2004 24 7859 7868 15356198 PMC6729936
- Carta M Olivera DS Dettmer TS Valenzuela CF Ethanol withdrawal upregulates kainate receptors in cultured rat hippocampal neurons Neurosci Lett 2002 327 128 132 12098652
- Cebere A Cebers G Liljequist S Enhancement of NMDA-induced functional responses without concomitant NMDA receptor changes following chronic ethanol exposure in cerebellar granule cells Naunyn Schmiedebergs Arch Pharmacol 1999 360 623 632 10619178
- Chandler LJ Harris RA Crews FT Ethanol tolerance and synaptic plasticity Trends Pharmacol Sci 1998 19 491 495 9871410
- Chandler LJ Newsom H Sumners C Crews F Chronic ethanol exposure potentiates NMDA excitotoxicity in cerebral cortical neurons J Neurochem 1993 60 1578 1581 8455043
- Chandler LJ Norwood D Sutton G Chronic ethanol upregulates NMDA and AMPA, but not kainate receptor subunit proteins in rat primary cortical cultures Alcohol Clin Exp Res 1999 23 363 370 10069569
- Chandler LJ Sutton G Norwood D Sumners C Crews FT Chronic ethanol increases N-methyl-D-aspartate-stimulated nitric oxide formation but not receptor density in cultured cortical neurons Mol Pharmacol 1997 51 733 740 9145911
- Chandra D Jia F Liang J Peng Z Suryanarayanan A Werner DF Spigelman I Houser CR Olsen RW Harrison NL Homanics GE GABAA receptor alpha 4 subunits mediate extrasynaptic inhibition in thalamus and dentate gyrus and the action of gaboxadol Proc Natl Acad Sci U S A 2006 103 15230 15235 17005728 PMC1578762
- Charlton ME Sweetnam PM Fitzgerald LW Terwilliger RZ Nestler EJ Duman RS Chronic ethanol administration regulates the expression of GABAA receptor alpha 1 and alpha 5 subunits in the ventral tegmental area and hippocampus J Neurochem 1997 68 121 127 8978717
- Cherubini E Conti F Generating diversity at GABAergic synapses Trends Neurosci 2001 24 155 162 11182455
- Christian DT Alexander NJ Diaz MR McCool BA Thalamic glutamatergic afferents into the rat basolateral amygdala exhibit increased presynaptic glutamate function following withdrawal from chronic intermittent ethanol Neuropharmacology 2013 65 134 142 22982568 PMC3521082
- Christian DT Alexander NJ Diaz MR Robinson S McCool BA Chronic intermittent ethanol and withdrawal differentially modulate basolateral amygdala AMPA-type glutamate receptor function and trafficking Neuropharmacology 2012 62 2430 2439 22387532 PMC3314101
- Chu B Anantharam V Treistman SN Ethanol inhibition of recombinant heteromeric NMDA channels in the presence and absence of modulators J Neurochem 1995 65 140 148 7540660
- Churn SB Rana A Lee K Parsons JT De Blas A Delorenzo RJ Calcium/calmodulin-dependent kinase II phosphorylation of the GABAA receptor alpha1 subunit modulates benzodiazepine binding J Neurochem 2002 82 1065 1076 12358754
- Collingridge GL Olsen RW Peters J Spedding M A nomenclature for ligand-gated ion channels Neuropharmacology 2009 56 2 5 18655795 PMC2847504
- Colombo G Agabio R Carai MA Lobina C Pani M Reali R Addolorato G Gessa GL Ability of baclofen in reducing alcohol intake and withdrawal severity: I--Preclinical evidence Alcohol Clin Exp Res 2000 24 58 66 10656194
- Costa ET Soto EE Cardoso RA Olivera DS Valenzuela CF Acute effects of ethanol on kainate receptors in cultured hippocampal neurons Alcohol Clin Exp Res 2000 24 220 225 10698375
- Cozzoli DK Courson J Caruana AL Miller BW Greentree DI Thompson AB Wroten MG Zhang PW Xiao B Hu JH Klugmann M Metten P Worley PF Crabbe JC Szumlinski KK Nucleus accumbens mGluR5-associated signaling regulates binge alcohol drinking under drinking-in-the-dark procedures Alcohol Clin Exp Res 2012 36 1623 1633 22432643 PMC3382009
- Cozzoli DK Courson J Wroten MG Greentree DI Lum EN Campbell RR Thompson AB Maliniak D Worley PF Jonquieres G Klugmann M Finn DA Szumlinski KK Binge alcohol drinking by mice requires intact group 1 metabotropic glutamate receptor signaling within the central nucleus of the amygdala Neuropsychopharmacology 2014 39 435 444 23966068 PMC3870786
- Cozzoli DK Goulding SP Zhang PW Xiao B Hu JH Ary AW Obara I Rahn A Abou-Ziab H Tyrrel B Marini C Yoneyama N Metten P Snelling C Dehoff MH Crabbe JC Finn DA Klugmann M Worley PF Szumlinski KK Binge drinking upregulates accumbens mGluR5-Homer2-PI3K signaling: functional implications for alcoholism J Neurosci 2009 29 8655 8668 19587272 PMC2761716
- Criswell HE Breese GR A conceptualization of integrated actions of ethanol contributing to its GABAmimetic profile: a commentary Neuropsychopharmacology 2005 30 1407 1425 15856077
- Criswell HE Ming Z Griffith BL Breese GR 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 2003 304 192 199 12490591
- Cruz MT Herman MA Kallupi M Roberto M Nociceptin/orphanin FQ blockade of corticotropin-releasing factor-induced gamma-aminobutyric acid release in central amygdala is enhanced after chronic ethanol exposure Biol Psychiatry 2012 71 666 676 22153590 PMC3838304
- Dahchour A De Witte P Effect of repeated ethanol withdrawal on glutamate microdialysate in the hippocampus Alcohol Clin Exp Res 1999 23 1698 1703 10550004
- Dahchour A De Witte P Excitatory and inhibitory amino acid changes during repeated episodes of ethanol withdrawal: an in vivo microdialysis study Eur J Pharmacol 2003 459 171 178 12524143
- Davis TJ de Fiebre CM Alcohol’s actions on neuronal nicotinic acetylcholine receptors Alcohol Res Health 2006 29 179 185 17373406 PMC6527039
- De Koninck Y Mody I Noise analysis of miniature IPSCs in adult rat brain slices: properties and modulation of synaptic GABAA receptor channels J Neurophysiol 1994 71 1318 1335 8035217
- Devaud LL Fritschy JM Sieghart W Morrow AL Bidirectional alterations of GABA(A) receptor subunit peptide levels in rat cortex during chronic ethanol consumption and withdrawal J Neurochem 1997 69 126 130 9202302
- Devaud LL Smith FD Grayson DR Morrow AL Chronic ethanol consumption differentially alters the expression of gamma-aminobutyric acidA receptor subunit mRNAs in rat cerebral cortex: competitive, quantitative reverse transcriptase-polymerase chain reaction analysis Mol Pharmacol 1995 48 861 868 7476917
- Diamond I Gordon AS The role of adenosine in mediating cellular and molecular responses to ethanol Exs 1994 71 175 183 8032148
- Dildy-Mayfield JE Harris RA Acute and chronic ethanol exposure alters the function of hippocampal kainate receptors expressed in Xenopus oocytes J Neurochem 1992 58 1569 1572 1312578
- Dildy JE Leslie SW Ethanol inhibits NMDA-induced increases in free intracellular Ca2+ in dissociated brain cells Brain Res 1989 499 383 387 2572303
- Dolphin AC Beta subunits of voltage-gated calcium channels J Bioenerg Biomembr 2003a 35 599 620 15000522
- Dolphin AC G protein modulation of voltage-gated calcium channels Pharmacol Rev 2003b 55 607 627 14657419
- Eckardt MJ File SE Gessa GL Grant KA Guerri C Hoffman PL Kalant H Koob GF Li TK Tabakoff B Effects of moderate alcohol consumption on the central nervous system Alcohol Clin Exp Res 1998 22 998 1040 9726269
- Eggers ED Berger AJ Mechanisms for the modulation of native glycine receptor channels by ethanol J Neurophysiol 2004 91 2685 2695 14762156
- Elmslie KS Neurotransmitter modulation of neuronal calcium channels J Bioenerg Biomembr 2003 35 477 489 15000517
- Enoch MA The role of GABA(A) receptors in the development of alcoholism Pharmacol Biochem Behav 2008 90 95 104 18440057 PMC2577853
- Enoch MA Zhou Z Kimura M Mash DC Yuan Q Goldman D GABAergic gene expression in postmortem hippocampus from alcoholics and cocaine addicts; corresponding findings in alcohol-naive P and NP rats PLoS One 2012 7 e29369 22253714 PMC3258238
- File SE Zharkovsky A Gulati K Effects of baclofen and nitrendipine on ethanol withdrawal responses in the rat Neuropharmacology 1991 30 183 190 2030822
- Floyd DW Friedman DP Daunais JB Pierre PJ Grant KA McCool BA Long-term ethanol self-administration by cynomolgus macaques alters the pharmacology and expression of GABAA receptors in basolateral amygdala J Pharmacol Exp Ther 2004 311 1071 1079 15280440
- Floyd DW Jung KY McCool BA Chronic ethanol ingestion facilitates N-methyl-D-aspartate receptor function and expression in rat lateral/basolateral amygdala neurons J Pharmacol Exp Ther 2003 307 1020 1029 14534353
- Follesa P Ticku MK Chronic ethanol treatment differentially regulates NMDA receptor subunit mRNA expression in rat brain Brain Res Mol Brain Res 1995 29 99 106 7770006
- Forstera B Castro PA Moraga-Cid G Aguayo LG Potentiation of Gamma Aminobutyric Acid Receptors (GABAAR) by Ethanol: How Are Inhibitory Receptors Affected? Front Cell Neurosci 2016 10 114 27199667 PMC4858537
- Frye GD Fincher A Sensitivity of postsynaptic GABAB receptors on hippocampal CA1 and CA3 pyramidal neurons to ethanol Brain Res 1996 735 239 248 8911662
- Frye GD Fincher A Sustained ethanol inhibition of native AMPA receptors on medial septum/diagonal band (MS/DB) neurons Br J Pharmacol 2000 129 87 94 10694206 PMC1621129
- Frye GD McCown TJ Breese GR Differential sensitivity of ethanol withdrawal signs in the rat to gamma-aminobutyric acid (GABA)mimetics: blockade of audiogenic seizures but not forelimb tremors J Pharmacol Exp Ther 1983 226 720 725 6310080
- Fujii S Yamazaki Y Sugihara T Wakabayashi I Acute and chronic ethanol exposure differentially affect induction of hippocampal LTP Brain Res 2008 1211 13 21 18423576
- Glykys J Peng Z Chandra D Homanics GE Houser CR Mody I A new naturally occurring GABA(A) receptor subunit partnership with high sensitivity to ethanol Nat Neurosci 2007 10 40 48 17159992
- Grobin AC Fritschy JM Morrow AL Chronic ethanol administration alters immunoreactivity for GABA(A) receptor subunits in rat cortex in a region-specific manner Alcohol Clin Exp Res 2000 24 1137 1144 10968650
- Grobin AC Matthews DB Devaud LL Morrow AL The role of GABA(A) receptors in the acute and chronic effects of ethanol Psychopharmacology (Berl) 1998 139 2 19 9768538
- Grover CA Frye GD Griffith WH Acute tolerance to ethanol inhibition of NMDA-mediated EPSPs in the CA1 region of the rat hippocampus Brain Res 1994 642 70 76 7913393
- Grover CA Wallace KA Lindberg SA Frye GD Ethanol inhibition of NMDA currents in acutely dissociated medial septum/diagonal band neurons from ethanol dependent rats Brain Res 1998 782 43 52 9519248
- Gulya K Grant KA Valverius P Hoffman PL Tabakoff B Brain regional specificity and time-course of changes in the NMDA receptor-ionophore complex during ethanol withdrawal Brain Res 1991 547 129 134 1830510
- Hanchar HJ Dodson PD Olsen RW Otis TS Wallner M Alcohol-induced motor impairment caused by increased extrasynaptic GABA(A) receptor activity Nat Neurosci 2005 8 339 345 15696164 PMC2854077
- Harris RA Ethanol actions on multiple ion channels: which are important? Alcohol Clin Exp Res 1999 23 1563 1570 10549986
- Harris RA Trudell JR Mihic SJ Ethanol’s molecular targets Sci Signal 2008 1 7 PMC2671803 18632551
- Heilig M Egli M Crabbe JC Becker HC Acute withdrawal, protracted abstinence and negative affect in alcoholism: are they linked? Addict Biol 2010 15 169 184 20148778 PMC3268458
- Herman MA Contet C Justice NJ Vale W Roberto M Novel subunit-specific tonic GABA currents and differential effects of ethanol in the central amygdala of CRF receptor-1 reporter mice J Neurosci 2013 33 3284 3298 23426657 PMC3711798
- Herman MA Roberto M Cell-type-specific tonic GABA signaling in the rat central amygdala is selectively altered by acute and chronic ethanol Addict Biol 2016 21 72 86 25170988 PMC4345144
- Herring D Huang R Singh M Robinson LC Dillon GH Leidenheimer NJ Constitutive GABAA receptor endocytosis is dynamin-mediated and dependent on a dileucine AP2 adaptin-binding motif within the beta 2 subunit of the receptor J Biol Chem 2003 278 24046 24052 12707262
- Hoffman PL Rabe CS Moses F Tabakoff B N-methyl-D-aspartate receptors and ethanol: inhibition of calcium flux and cyclic GMP production J Neurochem 1989 52 1937 1940 2542453
- Hu M Walker DW Vickroy TW Peris J Chronic ethanol exposure increases 3H–GABA release in rat hippocampus by presynaptic muscarinic receptor modulation Alcohol Clin Exp Res 1999 23 1587 1595 10549989
- Hu XJ Follesa P Ticku MK Chronic ethanol treatment produces a selective upregulation of the NMDA receptor subunit gene expression in mammalian cultured cortical neurons Brain Res Mol Brain Res 1996 36 211 218 8965641
- Hyytia P Koob GF GABAA receptor antagonism in the extended amygdala decreases ethanol self-administration in rats Eur J Pharmacol 1995 283 151 159 7498304
- Iorio KR Reinlib L Tabakoff B Hoffman PL Chronic exposure of cerebellar granule cells to ethanol results in increased N-methyl-D-aspartate receptor function Mol Pharmacol 1992 41 1142 1148 1535416
- Iorio KR Tabakoff B Hoffman PL Glutamate-induced neurotoxicity is increased in cerebellar granule cells exposed chronically to ethanol Eur J Pharmacol 1993 248 209 212 7901044
- Ives JH Drewery DL Thompson CL Differential cell surface expression of GABAA receptor alpha1, alpha6, beta2 and beta3 subunits in cultured mouse cerebellar granule cells influence of cAMP-activated signalling J Neurochem 2002 80 317 327 11902122
- Jia F Chandra D Homanics GE Harrison NL Ethanol modulates synaptic and extrasynaptic GABAA receptors in the thalamus J Pharmacol Exp Ther 2008 326 475 482 18477766 PMC2669290
- Jin C Smothers CT Woodward JJ Enhanced ethanol inhibition of recombinant N-methyl-D-aspartate receptors by magnesium: role of NR3A subunits Alcohol Clin Exp Res 2008 32 1059 1066 18445116 PMC3590455
- Jin C Woodward JJ Effects of 8 different NR1 splice variants on the ethanol inhibition of recombinant NMDA receptors Alcohol Clin Exp Res 2006 30 673 679 16573586
- Kalivas PW The glutamate homeostasis hypothesis of addiction Nat Rev Neurosci 2009 10 561 572 19571793
- Kang J Jiang L Goldman SA Nedergaard M Astrocyte-mediated potentiation of inhibitory synaptic transmission Nat Neurosci 1998a 1 683 692 10196584
- Kang M Spigelman I Sapp DW Olsen RW Persistent reduction of GABA(A) receptor-mediated inhibition in rat hippocampus after chronic intermittent ethanol treatment Brain Res 1996 709 221 228 8833758
- Kang MH Spigelman I Olsen RW Alteration in the sensitivity of GABA(A) receptors to allosteric modulatory drugs in rat hippocampus after chronic intermittent ethanol treatment Alcohol Clin Exp Res 1998b 22 2165 2173 9884165
- Kash TL Baucum AJ 2nd Conrad KL Colbran RJ Winder DG Alcohol exposure alters NMDAR function in the bed nucleus of the stria terminalis Neuropsychopharmacology 2009 34 2420 2429 19553918 PMC2864644
- Kash TL Matthews RT Winder DG Alcohol inhibits NR2B-containing NMDA receptors in the ventral bed nucleus of the stria terminalis Neuropsychopharmacology 2008 33 1379 1390 17625498 PMC2864636
- Kelm MK Criswell HE Breese GR Calcium release from presynaptic internal stores is required for ethanol to increase spontaneous gamma-aminobutyric acid release onto cerebellum Purkinje neurons J Pharmacol Exp Ther 2007 323 356 364 17652632
- Kelm MK Criswell HE Breese GR The role of protein kinase A in the ethanol-induced increase in spontaneous GABA release onto cerebellar Purkinje neurons J Neurophysiol 2008 100 3417 3428 18945815 PMC2604841
- Kelm MK Criswell HE Breese GR Ethanol-enhanced GABA release: a focus on G protein-coupled receptors Brain Res Rev 2011 65 113 123 20837058 PMC3005894
- Kittler JT Chen G Kukhtina V Vahedi-Faridi A Gu Z Tretter V Smith KR McAinsh K Arancibia-Carcamo IL Saenger W Haucke V Yan Z Moss SJ Regulation of synaptic inhibition by phospho-dependent binding of the AP2 complex to a YECL motif in the GABAA receptor gamma2 subunit Proc Natl Acad Sci U S A 2008 105 3616 3621 18305175 PMC2265186
- Kliethermes CL Anxiety-like behaviors following chronic ethanol exposure Neurosci Biobehav Rev 2005 28 837 850 15642625
- Knapp DJ Overstreet DH Breese GR Baclofen blocks expression and sensitization of anxiety-like behavior in an animal model of repeated stress and ethanol withdrawal Alcohol Clin Exp Res 2007 31 582 595 17374037 PMC2864137
- Koob GF Alcoholism: allostasis and beyond Alcohol Clin Exp Res 2003 27 232 243 12605072
- Koob GF Neurobiological substrates for the dark side of compulsivity in addiction Neuropharmacology 56 Suppl 2009 1 18 31 PMC2637927 18725236
- Koob GF Volkow ND Neurocircuitry of addiction Neuropsychopharmacology 2010 35 217 238 19710631 PMC2805560
- Kroener S Mulholland PJ New NN Gass JT Becker HC Chandler LJ Chronic alcohol exposure alters behavioral and synaptic plasticity of the rodent prefrontal cortex PLoS One 2012 7 e37541 22666364 PMC3364267
- Kumar S Fleming RL Morrow AL Ethanol regulation of gamma-aminobutyric acid A receptors: genomic and nongenomic mechanisms Pharmacol Ther 2004 101 211 226 15031000
- Kumar S Kralic JE O’Buckley TK Grobin AC Morrow AL Chronic ethanol consumption enhances internalization of alpha1 subunit-containing GABAA receptors in cerebral cortex J Neurochem 2003 86 700 708 12859683
- Kumar S Porcu P Werner DF Matthews DB Diaz-Granados JL Helfand RS Morrow AL The role of GABA(A) receptors in the acute and chronic effects of ethanol: a decade of progress Psychopharmacology (Berl) 2009 PMC2814770 19455309
- Kumar S Sieghart W Morrow AL Association of protein kinase C with GABA(A) receptors containing alpha1 and alpha4 subunits in the cerebral cortex: selective effects of chronic ethanol consumption J Neurochem 2002 82 110 117 12091471
- Kuner T Schoepfer R Korpi ER Ethanol inhibits glutamate-induced currents in heteromeric NMDA receptor subtypes Neuroreport 1993 5 297 300 7905294
- Lack AK Ariwodola OJ Chappell AM Weiner JL McCool BA Ethanol inhibition of kainate receptor-mediated excitatory neurotransmission in the rat basolateral nucleus of the amygdala Neuropharmacology 2008 55 661 668 18617194 PMC2615485
- Lack AK Christian DT Diaz MR McCool BA Chronic ethanol and withdrawal effects on kainate receptor-mediated excitatory neurotransmission in the rat basolateral amygdala Alcohol 2009 43 25 33 19185207 PMC2662731
- Lack AK Diaz MR Chappell A DuBois DW McCool BA Chronic ethanol and withdrawal differentially modulate pre- and postsynaptic function at glutamatergic synapses in rat basolateral amygdala J Neurophysiol 2007 98 3185 3196 17898152 PMC2269699
- Lack AK Floyd DW McCool BA Chronic ethanol ingestion modulates proanxiety factors expressed in rat central amygdala Alcohol 2005 36 83 90 16396741 PMC1557647
- Liang J Cagetti E Olsen RW Spigelman I Altered pharmacology of synaptic and extrasynaptic GABAA receptors on CA1 hoppocampal neurons is consistent with subunit changes in a model of alcohol withdrawal and dependence J Pharmacol Exp Ther 2004 4 4 15126642
- Liang J Lindemeyer AK Suryanarayanan A Meyer EM Marty VN Ahmad SO Shao XM Olsen RW Spigelman I Plasticity of GABA(A) receptor-mediated neurotransmission in the nucleus accumbens of alcohol-dependent rats J Neurophysiol 2014 112 39 50 24694935 PMC4152163
- Liang J Spigelman I Olsen RW Tolerance to sedative/hypnotic actions of GABAergic drugs correlates with tolerance to potentiation of extrasynaptic tonic currents of alcohol-dependent rats J Neurophysiol 2009 102 224 233 19420124 PMC2712270
- Lima-Landman MT Albuquerque EX Ethanol potentiates and blocks NMDA-activated single-channel currents in rat hippocampal pyramidal cells FEBS Lett 1989 247 61 67 2468533
- Lobo IA Harris RA GABA(A) receptors and alcohol Pharmacol Biochem Behav 2008 90 90 94 18423561 PMC2574824
- Lovinger DM 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 1995 274 164 172 7616394
- Lovinger DM Alcohols and neurotransmitter gated ion channels: past, present and future Naunyn Schmiedebergs Arch Pharmacol 1997 356 267 282 9303562
- Lovinger DM Homanics GE Tonic for what ails us? high-affinity GABAA receptors and alcohol Alcohol 2007 41 139 143 17521844 PMC2043151
- Lovinger DM Roberto M Sommer WH Spanagel R Synaptic Effects Induced by Alcohol Current Topics in Behavioral Neurosciences 2013 13 Springer-Verlag Berlin-Heidelberg 31 86 PMC4791588 21786203
- Lovinger DM White G Weight FF Ethanol inhibits NMDA-activated ion current in hippocampal neurons Science 1989 243 1721 1724 2467382
- Lovinger DM White G Weight FF NMDA receptor-mediated synaptic excitation selectively inhibited by ethanol in hippocampal slice from adult rat J Neurosci 1990 10 1372 1379 2158533 PMC6570208
- Lu SM Yeh HH Ethanol modulates AMPA-induced current responses of primary somatosensory cortical neurons Neurochem Int 1999 35 175 183 10406001
- Luthin GR Tabakoff B Activation of adenylate cyclase by alcohols requires the nucleotide-binding protein J Pharmacol Exp Ther 1984 228 579 587 6707909
- Mahmoudi M Kang MH Tillakaratne N Tobin AJ Olsen RW Chronic intermittent ethanol treatment in rats increases GABA(A) receptor alpha4-subunit expression: possible relevance to alcohol dependence J Neurochem 1997 68 2485 2492 9166743
- Mameli M Zamudio PA Carta M Valenzuela CF Developmentally regulated actions of alcohol on hippocampal glutamatergic transmission J Neurosci 2005 25 8027 8036 16135760 PMC6725449
- Marszalec W Kurata Y Hamilton BJ Carter DB Narahashi T Selective effects of alcohols on gamma-aminobutyric acid A receptor subunits expressed in human embryonic kidney cells J Pharmacol Exp Ther 1994 269 157 163 7513357
- Marty VN Spigelman I 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 Front Neurosci 2012 6 86 22701402 PMC3370662
- Marutha Ravindran CR Mehta AK Ticku MK Effect of chronic administration of ethanol on the regulation of the delta-subunit of GABA(A) receptors in the rat brain Brain Res 2007 1174 47 52 17854781 PMC2278031
- Masood K Wu C Brauneis U Weight FF Differential ethanol sensitivity of recombinant N-methyl-D-aspartate receptor subunits Mol Pharmacol 1994 45 324 329 8114679
- Matthews DB Devaud LL Fritschy JM Sieghart W Morrow AL Differential regulation of GABA(A) receptor gene expression by ethanol in the rat hippocampus versus cerebral cortex J Neurochem 1998 70 1160 1166 9489737
- McCool BA Frye GD Pulido MD Botting SK Effects of chronic ethanol consumption on rat GABA(A) and strychnine-sensitive glycine receptors expressed by lateral/basolateral amygdala neurons Brain Res 2003 963 165 177 12560122 PMC2925189
- McCown TJ Breese GR Multiple withdrawals from chronic ethanol “kindles” infrior collicular seizure activity: Evidence for kindling seizures associated with alcoholism Alcohol. Clin. Exp. Res 1990 14 394 399 2378423
- McCown TJ Frye GD Breese GR Evidence for site specific ethanol actions in the CNS Alcohol Drug Res 1985 6 423 429 3939188
- McKernan RM Whiting PJ Which GABAA-receptor subtypes really occur in the brain? Trends Neurosci 1996 19 139 143 8658597
- Melendez RI Hicks MP Cagle SS Kalivas PW Ethanol exposure decreases glutamate uptake in the nucleus accumbens Alcohol Clin Exp Res 2005a 29 326 333 15770106
- Melendez RI Vuthiganon J Kalivas PW Regulation of extracellular glutamate in the prefrontal cortex: focus on the cystine glutamate exchanger and group I metabotropic glutamate receptors J Pharmacol Exp Ther 2005b 314 139 147 15769865
- Mhatre M Ticku MK Chronic ethanol treatment upregulates the GABA receptor beta subunit expression Brain Res Mol Brain Res 1994 23 246 252 8057781
- Mihic SJaHRA Deitrich R Erwin VG Alcohol actions at the GABAA receptor/chloride channel complex Pharmacological effect of ethanol on the neurvous system 1996 Boca Raton CRC press 51 72
- Ming Z Criswell HE Yu G Breese GR Competing presynaptic and postsynaptic effects of ethanol on cerebellar purkinje neurons Alcohol Clin Exp Res 2006 30 1400 1407 16899043 PMC2949273
- Miyakawa T Yagi T Kitazawa H Yasuda M Kawai N Tsuboi K Niki H Fyn-kinase as a determinant of ethanol sensitivity: relation to NMDA-receptor function Science 1997 278 698 701 9381182
- Mohler H Fritschy JM Luscher B Rudolph U Benson J Benke D The GABAA receptors. From subunits to diverse functions Ion Channels 1996 4 89 113 8744207
- Morrisett RA Swartzwelder HS Attenuation of hippocampal long-term potentiation by ethanol: a patch-clamp analysis of glutamatergic and GABAergic mechanisms J Neurosci 1993 13 2264 2272 8478698 PMC6576561
- Morrow AL Devaud LL Bucci D Smith FD GABAA and NMDA receptor subunit mRNA expression in ethanol dependent rats Alcohol Alcohol Suppl 1994 2 89 95 8974321
- Morrow AL Herbert JS Montpied P Differential effects of chronic ethanol administration on GABA(A) receptor alpha1 and alpha6 subunit mRNA levels in rat cerebellum Mol Cell Neurosci 1992 3 251 258 19912867
- Morrow AL Suzdak PD Karanian JW Paul SM Chronic ethanol administration alters gamma-aminobutyric acid, pentobarbital and ethanol-mediated 36Cl- uptake in cerebral cortical synaptoneurosomes J Pharmacol Exp Ther 1988 246 158 164 2839659
- Moykkynen T Korpi ER Lovinger DM 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 2003 306 546 555 12734392
- Moykkynen TP Coleman SK Keinanen K Lovinger DM Korpi ER Ethanol increases desensitization of recombinant GluR-D AMPA receptor and TARP combinations Alcohol 2009 43 277 284 19560629 PMC2704482
- Netzeband JG Schneeloch JR Trotter C Caguioa-Aquino JN Gruol DL Chronic ethanol treatment and withdrawal alter ACPD-evoked calcium signals in developing Purkinje neurons Alcohol Clin Exp Res 2002 26 386 393 11923593
- Netzeband JG Trotter C Caguioa JN Gruol DL Chronic ethanol exposure enhances AMPA-elicited Ca2+ signals in the somatic and dendritic regions of cerebellar Purkinje neurons Neurochem Int 1999 35 163 174 10406000
- Newton PM Messing RO Intracellular signaling pathways that regulate behavioral responses to ethanol Pharmacol Ther 2006 109 227 237 16102840
- Nie Z Madamba SG Siggins GR Ethanol enhances gamma-aminobutyric acid responses in a subpopulation of nucleus accumbens neurons: role of metabotropic glutamate receptors J Pharmacol Exp Ther 2000 293 654 661 10773041
- Nie Z Yuan X Madamba SG Siggins GR Ethanol decreases glutamatergic synaptic transmission in rat nucleus accumbens in vitro: naloxone reversal J Pharmacol Exp Ther 1993 266 1705 1712 8396641
- Nieber K Poelchen W Sieler D Illes P Inhibition by ethanol of excitatory amino acid receptors in rat locus coeruleus neurons in vitro Naunyn Schmiedebergs Arch Pharmacol 1998 357 299 308 9550302
- Obara I Bell RL Goulding SP Reyes CM Larson LA Ary AW Truitt WA Szumlinski KK Differential effects of chronic ethanol consumption and withdrawal on homer/glutamate receptor expression in subregions of the accumbens and amygdala of P rats Alcohol Clin Exp Res 2009 33 1924 1934 19673743 PMC2873844
- Ortiz J Fitzgerald LW Charlton M Lane S Trevisan L Guitart X Shoemaker W Duman RS Nestler EJ Biochemical actions of chronic ethanol exposure in the mesolimbic dopamine system Synapse 1995 21 289 298 8869159
- Otis TS De Koninck Y Mody I Lasting potentiation of inhibition is associated with an increased number of gamma-aminobutyric acid type A receptors activated during miniature inhibitory postsynaptic currents Proc Natl Acad Sci U S A 1994 91 7698 7702 8052645 PMC44469
- Papadeas S Grobin AC Morrow AL Chronic ethanol consumption differentially alters GABA(A) receptor alpha1 and alpha4 subunit peptide expression and GABA(A) receptor-mediated 36 Cl(-) uptake in mesocorticolimbic regions of rat brain Alcohol Clin Exp Res 2001 25 1270 1275 11584145
- Pati D Kelly K Stennett B Frazier CJ Knackstedt LA Alcohol consumption increases basal extracellular glutamate in the nucleus accumbens core of Sprague-Dawley rats without increasing spontaneous glutamate release Eur J Neurosci 2016 44 1896 1905 27207718 PMC5620661
- Peris J Eppler B Hu M Walker DW Hunter BE Mason K Anderson KJ Effects of chronic ethanol exposure on GABA receptors and GABAB receptor modulation of 3H–GABA release in the hippocampus Alcohol Clin Exp Res 1997 21 1047 1052 9309316
- Pirker S Schwarzer C Wieselthaler A Sieghart W Sperk G GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain Neuroscience 2000 101 815 850 11113332
- Pleil KE Lowery-Gionta EG Crowley NA Li C Marcinkiewcz CA Rose JH McCall NM Maldonado-Devincci AM Morrow AL Jones SR Kash TL Effects of chronic ethanol exposure on neuronal function in the prefrontal cortex and extended amygdala Neuropharmacology 2015 99 735 749 26188147 PMC4781662
- Ponomarev I Wang S Zhang L Harris RA Mayfield RD Gene coexpression networks in human brain identify epigenetic modifications in alcohol dependence J Neurosci 2012 32 1884 1897 22302827 PMC3564514
- Rabin RA Molinoff PB Activation of adenylate cyclase by ethanol in mouse striatal tissue J Pharmacol Exp Ther 1981 216 129 134 7452500
- Rao PS Bell RL Engleman EA Sari Y Targeting glutamate uptake to treat alcohol use disorders Front Neurosci 2015 9 144 25954150 PMC4407613
- Ren H Zhao Y Wu M Peoples RW A novel alcohol-sensitive position in the N-methyl-D-aspartate receptor GluN2A subunit M3 domain regulates agonist affinity and ion channel gating Mol Pharmacol 2013 84 501 510 23847085 PMC3781384
- Renteria R Maier EY Buske TR Morrisett RA Selective alterations of NMDAR function and plasticity in D1 and D2 medium spiny neurons in the nucleus accumbens shell following chronic intermittent ethanol exposure Neuropharmacology 2016 PMC5755972 26946430
- Roberto M Bajo M Crawford E Madamba SG Siggins GR Chronic ethanol exposure and protracted abstinence alter NMDA receptors in central amygdala Neuropsychopharmacology 2006 31 988 996 16052244
- Roberto M Cruz MT Gilpin NW Sabino V Schweitzer P Bajo M Cottone P Madamba SG Stouffer DG Zorrilla EP Koob GF Siggins GR Parsons LH Corticotropin Releasing Factor-Induced Amygdala Gamma-Aminobutyric Acid Release Plays a Key Role in Alcohol Dependence Biol Psychiatry 2010 831 839 20060104 PMC2883449
- Roberto M Gilpin NW Noronha A Cui C Harris A Crabbe J Central amygdala neuroplasticity in alcohol dependence. In “Neurobiology of Alcohol Dependence” Section II, Neurocircuitry and Neurosignaling of Alcohol Dependence 2014 Elsevier Press 207 220
- Roberto M Madamba SG Moore SD Tallent MK Siggins GR Ethanol increases GABAergic transmission at both pre- and postsynaptic sites in rat central amygdala neurons Proc Natl Acad Sci U S A 2003 100 2053 2058 12566570 PMC149957
- Roberts AJ Cole M Koob GF Intra-amygdala muscimol decreases operant ethanol self-administration in dependent rats Alcohol Clin Exp Res 1996 20 1289 1298 8904984
- Ron D Barak S Molecular mechanisms underlying alcohol-drinking behaviours Nat Rev Neurosci 2016 17 576 591 27444358 PMC5131788
- Rossetti ZL Carboni S Ethanol withdrawal is associated with increased extracellular glutamate in the rat striatum Eur J Pharmacol 1995 283 177 183 7498307
- Sebe JY Eggers ED Berger AJ Differential effects of ethanol on GABA(A) and glycine receptor-mediated synaptic currents in brain stem motoneurons J Neurophysiol 2003 90 870 875 12702707
- Siggins GR Roberto M Nie Z The tipsy terminal: presynaptic effects of ethanol Pharmacol Ther 2005 107 80 98 15963352
- Smothers CT Mrotek JJ Lovinger DM Chronic ethanol exposure leads to a selective enhancement of N-methyl-D-aspartate receptor function in cultured hippocampal neurons J Pharmacol Exp Ther 1997 283 1214 1222 9399996
- Snell LD Nunley KR Lickteig RL Browning MD Tabakoff B Hoffman PL Regional and subunit specific changes in NMDA receptor mRNA and immunoreactivity in mouse brain following chronic ethanol ingestion Brain Res Mol Brain Res 1996 40 71 78 8840015
- Szumlinski KK Ary AW Lominac KD Klugmann M Kippin TE Accumbens Homer2 overexpression facilitates alcohol-induced neuroplasticity in C57BL/6J mice Neuropsychopharmacology 2008 33 1365 1378 17568396 PMC5099135
- Szumliski K Woodward JJ Noronha A Cui C Harris A Crabbe J Glutamate Signaling in Alcohol Abuse and Dependence Section II, Neurocircuitry and Neurosignaling of Alcohol Dependence 2014 Elsevier Press 173 206
- Talani G Lovinger DM Interactions between ethanol and the endocannabinoid system at GABAergic synapses on basolateral amygdala principal neurons Alcohol 2015 49 781 794 26603632 PMC4691436
- Terunuma M Xu J Vithlani M Sieghart W Kittler J Pangalos M Haydon PG Coulter DA Moss SJ Deficits in phosphorylation of GABA(A) receptors by intimately associated protein kinase C activity underlie compromised synaptic inhibition during status epilepticus J Neurosci 2008 28 376 384 18184780 PMC2917223
- Theile JW Morikawa H Gonzales RA Morrisett RA Ethanol enhances GABAergic transmission onto dopamine neurons in the ventral tegmental area of the rat Alcohol Clin Exp Res 2008 32 1040 1048 18422836 PMC2553853
- Ticku MK Burch T Alterations in gamma-aminobutyric acid receptor sensitivity following acute and chronic ethanol treatments J Neurochem 1980 34 417 423 6251168
- Tonner PH Miller KW Molecular sites of general anaesthetic action on acetylcholine receptors Eur J Anaesthesiol 1995 12 21 30 7535690
- Trantham-Davidson H Burnett EJ Gass JT Lopez MF Mulholland PJ Centanni SW Floresco SB Chandler LJ Chronic alcohol disrupts dopamine receptor activity and the cognitive function of the medial prefrontal cortex J Neurosci 2014 34 3706 3718 24599469 PMC3942586
- Trantham-Davidson H Centanni SW Garr SC New NN Mulholland PJ Gass JT Glover EJ Floresco SB Crews FT Krishnan HR Pandey SC Chandler LJ Binge-Like Alcohol Exposure during Adolescence Disrupts Dopaminergic Neurotransmission in the Adult Prelimbic Cortex Neuropsychopharmacology 2016 PMC5506791 27620551
- Tremwel MF Hunter BE Peris J Chronic ethanol exposure enhances [3H]GABA release and does not affect GABAA receptor mediated 36Cl uptake Synapse 1994 17 149 154 7974196
- Trevisan L Fitzgerald LW Brose N Gasic GP Heinemann SF Duman RS Nestler EJ Chronic ingestion of ethanol up-regulates NMDAR1 receptor subunit immunoreactivity in rat hippocampus J Neurochem 1994 62 1635 1638 8133290
- Tsai G Coyle JT The role of glutamatergic neurotransmission in the pathophysiology of alcoholism Annu Rev Med 1998 49 173 184 9509257
- Valenzuela CF Bhave S Hoffman P Harris RA Acute effects of ethanol on pharmacologically isolated kainate receptors in cerebellar granule neurons: comparison with NMDA and AMPA receptors J Neurochem 1998 71 1777 1780 9751216
- Valenzuela CF Jotty K Mini-Review: Effects of Ethanol on GABAA Receptor-Mediated Neurotransmission in the Cerebellar Cortex--Recent Advances Cerebellum 2015 14 438 446 25575727
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- Authors
- Roberto, M., & Varodayan, F. P.
- Affiliations
- Scripps Research Institute (US)
- Corresponding author
- Roberto, Marisa
- Venue
- Neuropharmacology
- Publisher
- Elsevier BV
- Published
- 2017-08
- Volume
- 122
- Pages
- 85-99
- ISSN
- 0028-3908 (ISSN-L)
- PMC
- PMC5479718
- OpenAlex
- W2573867270
- Cited by
- 149
- References
- 241
- Citations by year
- 2026: 7 · 2025: 6 · 2024: 9 · 2023: 11 · 2022: 23 · 2021: 26 · 2020: 21 · 2019: 22 · 2018: 19 · 2017: 5
- FWCI
- 2.29
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Neuropharmacology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Alcohol Abuse and Alcoholism (AA015566, AA006420, AA016985, AA017447, AA021491, AA013498)
- Pearson Center for Alcoholism and Addiction Research
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
- Keywords
- chronic ethanol exposure, synaptic plasticity, neural adaptation, alcohol withdrawal, alcoholism, glutamate, GABA, excitatory neurotransmission, inhibitory neurotransmission, synaptic proteins, alcohol reinforcement, synaptic transmission
- MeSH terms
- Ethanol, Alcoholism, Animals, Brain, gamma-Aminobutyric Acid, Humans, Synaptic Transmission, Neurons, Synapses, Glutamic Acid
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