Ethanol-enhanced GABA release: A focus on G protein-coupled receptors

Brain Research Reviews

Volumn 65, Issue 2, 2011, Pages 113-123

  Kelm, M Katherine ^a   Criswell, Hugh E ^a   Breese, George R ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Ethanol; G protein coupled receptor; GABA release; Internal calcium store; Presynaptic

Indexed keywords

2',3' DIDEOXYADENOSINE; 4 AMINOBUTYRIC ACID A RECEPTOR; 9 (TETRAHYDRO 2 FURYL)ADENINE; ADENOSINE TRIPHOSPHATE; ALCOHOL; BACLOFEN; CALPHOSTIN C; CHELERYTHRINE; CORTICOTROPIN RELEASING FACTOR; CYCLIC AMP; EDELFOSINE; FENCLONINE; G PROTEIN COUPLED RECEPTOR; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; NALTREXONE; NOCICEPTIN; NOCICEPTIN RECEPTOR; PRAZOSIN; PROTEIN KINASE C; RYANODINE RECEPTOR; SEROTONIN; TETRODOTOXIN; VOLTAGE GATED SODIUM CHANNEL;

4 AMINOBUTYRIC ACID RELEASE; ACTION POTENTIAL; ALCOHOL BLOOD LEVEL; ALCOHOL WITHDRAWAL; ALCOHOLISM; BRAIN REGION; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; DIALYSATE LEVEL; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; EVOKED RESPONSE; HORMONE INHIBITION; INHIBITORY POSTSYNAPTIC POTENTIAL; INTRACELLULAR SIGNALING; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; PURKINJE CELL; RECEPTOR BINDING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SYNAPTOSOME; TISSUE SPECIFICITY; VOLTAGE CLAMP; WHOLE CELL;

ANIMALS; BRAIN; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; GAMMA-AMINOBUTYRIC ACID; HUMANS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, GABA; SYNAPSES;

EID: 78649934510     PISSN: 01650173     EISSN: 18726321     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2010.09.003     Document Type: Review

References (95)

1. Addolorato G., Caputo F., Capristo E., Domenicali M., Bernardi M., Janiri L., Agabio R., Colombo G., Gessa G.L., Gasbarrini G. Baclofen efficacy in reducing alcohol craving and intake: a preliminary double-blind randomized controlled study. Alcohol Alcohol. 2002, 37:504-508.
2. Addolorato G., Leggio L., Ferrulli A., Cardone S., Vonghia L., Mirijello A., Abenavoli L., D'Angelo C., Caputo F., Zambon A., Haber P.S., Gasbarrini G. Effectiveness and safety of baclofen for maintenance of alcohol abstinence in alcohol-dependent patients with liver cirrhosis: randomised, double-blind controlled study. Lancet 2007, 370:1915-1922.
3. Ariwodola O.J., Weiner J.L. Ethanol potentiation of GABAergic synaptic transmission may be self-limiting: role of presynaptic GABA(B) receptors. J. Neurosci. 2004, 24:10679-10686.
4. Bajo M., Cruz M.T., Siggins G.R., Messing R., Roberto M. Protein kinase C epsilon mediation of CRF- and ethanol-induced GABA release in central amygdala. Proc. Natl. Acad. Sci. USA 2008, 105:8410-8415.
5. Bardo S., Robertson B., Stephens G.J. Presynaptic internal Ca2+ stores contribute to inhibitory neurotransmitter release onto mouse cerebellar Purkinje cells. Br. J. Pharmacol. 2002, 137:529-537.
6. Bardo S., Cavazzini M.G., Emptage N. The role of the endoplasmic reticulum Ca2+ store in the plasticity of central neurons. Trends Pharmacol. Sci. 2006, 27:78-84.
7. Benjamin D., Grant E.R., Pohorecky L.A. Naltrexone reverses ethanol-induced dopamine release in the nucleus accumbens in awake, freely moving rats. Brain Res. 1993, 621:137-140.
8. Boczan J., Leenders A.G., Sheng Z.H. Phosphorylation of syntaphilin by cAMP-dependent protein kinase modulates its interaction with syntaxin-1 and annuls its inhibitory effect on vesicle exocytosis. J. Biol. Chem. 2004, 279:18911-18919.
9. Bugrim A.E. Regulation of Ca2+ release by cAMP-dependent protein kinase. A mechanism for agonist-specific calcium signaling?. Cell Calcium 1999, 25:219-226.
10. Carlen P.L., Gurevich N., Durand D. Ethanol in low doses augments calcium-mediated mechanisms measured intracellularly in hippocampal neurons. Science 1982, 215:306-309.
11. Carta M., Mameli M., Valenzuela C.F. Alcohol enhances GABAergic transmission to cerebellar granule cells via an increase in Golgi cell excitability. J. Neurosci. 2004, 24:3746-3751.
12. Celada P., Paladini C.A., Tepper J.M. GABAergic control of rat substantia nigra dopaminergic neurons: role of globus pallidus and substantia nigra pars reticulata. Neuroscience 1999, 89:813-825.
13. Cheng G., Gao B., Verbny Y., Ziskind-Conhaim L. Ethanol reduces neuronal excitability and excitatory synaptic transmission in the developing rat spinal cord. Brain Res. 1999, 845:224-231.
14. Criswell H.E., Breese G.R. A conceptualization of integrated actions of ethanol contributing to its GABAmimetic profile: a commentary. Neuropsychopharmacology 2005, 30:1407-1425.
15. Criswell H.E., Ming Z., Kelm M.K., Breese G.R. Brain regional differences in the effect of ethanol on GABA release from presynaptic terminals. J. Pharmacol. Exp. Ther. 2008, 326:596-603.
16. Dahchour A., De Witte P. Effect of repeated ethanol withdrawal on glutamate microdialysate in the hippocampus. Alcohol. Clin. Exp. Res. 1999, 23:1698-1703.
17. Dahchour A., De Witte P. Taurine blocks the glutamate increase in the nucleus accumbens microdialysate of ethanol-dependent rats. Pharmacol. Biochem. Behav. 2000, 65:345-350.
18. Das J., Pany S., Rahman G.M., Slater S.J. PKC epsilon has an alcohol-binding site in its second cysteine-rich regulatory domain. Biochem. J. 2009, 421:405-413.
19. Frye G.D., Breese G.R. GABAergic modulation of ethanol-induced motor impairment. J. Pharmacol. Exp. Ther. 1982, 223:750-756.
20. Garbutt J.C., Kampov-Polevoy A., Flannery B., Kalka-Juhl L., Gallop R. Placebo-controlled trial of baclofen in alcohol dependence. Abstract. Alcohol. Clin. Exp. Res. 2007, 31. # 209.
21. George D.T., Gilman J., Hersh J., Thorsell A., Herion D., Geyer C., Peng X., Kielbasa W., Rawlings R., Brandt J.E., Gehlert D.R., Tauscher J.T., Hunt S.P., Hommer D., Heilig M. Neurokinin 1 receptor antagonism as a possible therapy for alcoholism. Science 2008, 319:1536-1539.
22. Glitsch M.D. Spontaneous neurotransmitter release and Ca2+-how spontaneous is spontaneous neurotransmitter release?. Cell Calcium 2008, 43:9-15.
23. Gordon E.R. The effect of ethanol on the concentration of gamma-aminobutyric acid in the rat brain. Can. J. Physiol. Pharmacol. 1967, 45:915-918.
24. Hanoune J., Defer N. Regulation and role of adenylyl cyclase isoforms. Annu. Rev. Pharmacol. Toxicol. 2001, 41:145-174.
25. Herve D., Pickel V.M., Joh T.H., Beaudet A. Serotonin axon terminals in the ventral tegmental area of the rat: fine structure and synaptic input to dopaminergic neurons. Brain Res. 1987, 435:71-83.
26. Hirono M., Yamada M., Obata K. Ethanol enhances both action potential-dependent and action potential-independent GABAergic transmission onto cerebellar Purkinje cells. Neuropharmacology 2009, 57:109-120.
27. Hopkins A.L., Groom C.R. The druggable genome. Nat. Rev. Drug Discov. 2002, 1:727-730.
28. Huang M.M., Overstreet D.H., Knapp D.J., Angel R., Wills T.A., Navarro M., Rivier J., Vale W., Breese G.R. Corticotropin-releasing factor (CRF) sensitization of ethanol withdrawal-induced anxiety-like behavior is brain site specific and mediated by CRF-1 receptors: relation to stress-induced sensitization. J. Pharmacol. Exp. Ther. 2010, 332:298-307.
29. Jia F., Chandra D., Homanics G.E., Harrison N.L. Ethanol modulates synaptic and extrasynaptic GABAA receptors in the thalamus. J. Pharmacol. Exp. Ther. 2008, 326:475-482.
30. Johnson S.W., North R.A. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci. 1992, 12:483-488.
31. Kang-Park M.H., Kieffer B.L., Roberts A.J., Siggins G.R., Moore S.D. Presynaptic delta opioid receptors regulate ethanol actions in central amygdala. J. Pharmacol. Exp. Ther. 2007, 320:917-925.
32. Kang-Park M.H., Kieffer B.L., Roberts A.J., Roberto M., Madamba S.G., Siggins G.R., Moore S.D. Mu-opioid receptors selectively regulate basal inhibitory transmission in the central amygdala: lack of ethanol interactions. J. Pharmacol. Exp. Ther. 2009, 328:284-293.
33. Kelm M.K., Criswell H.E., Breese G.R. 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.
34. Kelm M.K., Criswell H.E., Breese G.R. 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.
35. Kelm M.K., Weinberg R.J., Criswell H., Breese G. The PLC/IP3R/PKC pathway is required for ethanol-enhanced GABA release. Neuropharmacology 2010, 58:1179-1186.
36. Kemppainen H., Raivio N., Nurmi H., Kiianmaa K. GABA and glutamate overflow in the VTA and ventral pallidum of alcohol-preferring AA and alcohol-avoiding ANA rats after ethanol. Alcohol Alcohol. 2010, 45:111-118.
37. Kiselyov K., Shin D.M., Muallem S. Signalling specificity in GPCR-dependent Ca2+ signalling. Cell. Signal. 2003, 15:243-253.
38. Krnjevic K., Phillis J.W. Iontophoretic studies of neurones in the mammalian cerebral cortex. J. Physiol. 1963, 165:274-304.
39. Kubota H., Katsurabayashi S., Moorhouse A.J., Murakami N., Koga H., Akaike N. GABAB receptor transduction mechanisms, and cross-talk between protein kinases A and C, in GABAergic terminals synapsing onto neurons of the rat nucleus basalis of Meynert. J. Physiol. 2003, 551:263-276.
40. Li Q., Wilson W.A., Swartzwelder H.S. Developmental differences in the sensitivity of spontaneous and miniature IPSCs to ethanol. Alcohol. Clin. Exp. Res. 2006, 30:119-126.
41. Lou X., Korogod N., Brose N., Schneggenburger R. Phorbol esters modulate spontaneous and Ca2+-evoked transmitter release via acting on both Munc13 and protein kinase C. J. Neurosci. 2008, 28:8257-8267.
42. Mameli M., Botta P., Zamudio P.A., Zucca S. Valenzuela, C.F., 2008. Ethanol decreases Purkinje neuron excitability by increasing GABA release in rat cerebellar slices. J. Pharmacol. Exp. Ther. 2008, 327:910-917.
43. Manto M., Laute M.A., Pandolfo M. Depression of extra-cellular GABA and increase of NMDA-induced nitric oxide following acute intra-nuclear administration of alcohol in the cerebellar nuclei of the rat. Cerebellum 2005, 4:230-238.
44. Martin D.L. Short-term control of GABA synthesis in brain. Prog. Biophys. Mol. Biol. 1993, 60:17-28.
45. Maycox P.R., Hell J.W., Jahn R. Amino acid neurotransmission: spotlight on synaptic vesicles. Trends Neurosci. 1990, 13:83-87.
46. McIntire S.L., Reimer R.J., Schuske K., Edwards R.H., Jorgensen E.M. Identification and characterization of the vesicular GABA transporter. Nature 1997, 389:870-876.
47. Melis M., Camarini R., Ungless M.A., Bonci A. Long-lasting potentiation of GABAergic synapses in dopamine neurons after a single in vivo ethanol exposure. J. Neurosci. 2002, 22:2074-2082.
48. Mignery G.A., Newton C.L., Archer B.T., Sudhof T.C. Structure and expression of the rat inositol 1, 4, 5-trisphosphate receptor. J. Biol. Chem. 1990, 265:12679-12685.
49. Ming Z., Criswell H.E., Yu G., Breese G.R. Competing presynaptic and postsynaptic effects of ethanol on cerebellar purkinje neurons. Alcohol. Clin. Exp. Res. 2006, 30:1400-1407.
50. Nie Z., Schweitzer P., Roberts A.J., Madamba S.G., Moore S.D., Siggins G.R. Ethanol augments GABAergic transmission in the central amygdala via CRF1 receptors. Science 2004, 303:1512-1514.
51. Nie Z., Zorrilla E.P., Madamba S.G., Rice K.C., Roberto M., Siggins G.R. Presynaptic CRF1 receptors mediate the ethanol enhancement of GABAergic transmission in the mouse central amygdala. ScientificWorldJournal 2009, 9:68-85.
52. Otsuka M., Iversen L.L., Hall Z.W., Kravitz E.A. Release of gamma-aminobutyric acid from inhibitory nerves of lobster. Proc. Natl. Acad. Sci. USA 1966, 56:1110-1115.
53. Overstreet D.H., Knapp D.J., Breese G.R. Modulation of multiple ethanol withdrawal-induced anxiety-like behavior by CRF and CRF1 receptors. Pharmacol. Biochem. Behav. 2004, 77:405-413.
54. Patterson R.L., Boehning D., Snyder S.H. Inositol 1, 4, 5-trisphosphate receptors as signal integrators. Annu. Rev. Biochem. 2004, 73:437-465.
55. Piepponen T.P., Kiianmaa K., Ahtee L. Effects of ethanol on the accumbal output of dopamine, GABA and glutamate in alcohol-tolerant and alcohol-nontolerant rats. Pharmacol. Biochem. Behav. 2002, 74:21-30.
56. Roberto M., Siggins G.R. Nociceptin/orphanin FQ presynaptically decreases GABAergic transmission and blocks the ethanol-induced increase of GABA release in central amygdala. Proc. Natl. Acad. Sci. USA 2006, 103:9715-9720.
57. Roberto M., Madamba S.G., Moore S.D., Tallent M.K., Siggins G.R. Ethanol increases GABAergic transmission at both pre- and postsynaptic sites in rat central amygdala neurons. Proc. Natl. Acad. Sci. USA 2003, 100:2053-2058.
58. Roberto M., Madamba S.G., Stouffer D.G., Parsons L.H., Siggins G.R. Increased GABA release in the central amygdala of ethanol-dependent rats. J. Neurosci. 2004, 24:10159-10166.
59. Roberto M., Treistman S.N., Pietrzykowski A.Z., Weiner J., Galindo R., Mameli M., Valenzuela F., Zhu P.J., Lovinger D., Zhang T.A., Hendricson A.H., Morrisett R., Siggins G.R. Actions of acute and chronic ethanol on presynaptic terminals. Alcohol. Clin. Exp. Res. 2006, 30:222-232.
60. Roberto M., Cruz M., Bajo M., Siggins G.R., Schweitzer P. Interactions of ethanol and cannabinoids on synaptic transmission in central amygdala. Abstract. Alcohol. Clin. Exp. Res. 2008, 32. # 48.
61. Roberto M., Cruz M.T., Gilpin N.W., Sabino V., Schweitzer P., Bajo M., Cottone P., Madamba S.G., Stouffer D.G., Zorrilla E.P., Koob G.F., Siggins G.R., Parsons L.H. Corticotropin releasing factor-induced amygdala gamma-aminobutyric acid release plays a key role in alcohol dependence. Biol. Psychiatry 2010, 67:831-839.
62. Roberts E., Kuriyama K. Biochemical-physiological correlations in studies of the gamma-aminobutyric acid system. Brain Res. 1968, 8:1-35.
63. Sagne C., El Mestikawy S., Isambert M.F., Hamon M., Henry J.P., Giros B., Gasnier B. Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases. FEBS Lett. 1997, 417:177-183.
64. Sanna E., Talani G., Busonero F., Pisu M.G., Purdy R.H., Serra M., Biggio G. Brain steroidogenesis mediates ethanol modulation of GABAA receptor activity in rat hippocampus. J. Neurosci. 2004, 24:6521-6530.
65. Sebe J.Y., Eggers E.D., Berger A.J. Differential effects of ethanol on GABA(A) and glycine receptor-mediated synaptic currents in brain stem motoneurons. J. Neurophysiol. 2003, 90:870-875.
66. Siggins, G.R., Nie, Z., Madamba, S., 1999. A metabotropic hypothesis for ethanol sensitivity of GABAergic and glutamatergic central synapses. In: The 'drunken' Synapse: Studies of Alcohol-Related Disorders. Vol., Y. Liu, W. Hunt, ed.^eds. Kluwer Academic/Plenum Publishers, New York, pp. 219.
67. Siggins G.R., Roberto M., Nie Z. The tipsy terminal: presynaptic effects of ethanol. Pharmacol. Ther. 2005, 107:80-98.
68. Silberman Y., Shi L., Brunso-Bechtold J.K., Weiner J.L. Distinct mechanisms of ethanol potentiation of local and paracapsular GABAergic synapses in the rat basolateral amygdala. J. Pharmacol. Exp. Ther. 2008, 324:251-260.
69. Silberman Y., Ariwodola O.J., Weiner J.L. Differential effects of GABAB autoreceptor activation on ethanol potentiation of local and lateral paracapsular GABAergic synapses in the rat basolateral amygdala. Neuropharmacology 2009, 56:886-895.
70. Simpson T.L., Saxon A.J., Meredith C.W., Malte C.A., McBride B., Ferguson L.C., Gross C.A., Hart K.L., Raskind M. A pilot trial of the alpha-1 adrenergic antagonist, prazosin, for alcohol dependence. Alcohol. Clin. Exp. Res. 2009, 33:255-263.
71. Smith A., Watson C.J., Frantz K.J., Eppler B., Kennedy R.T., Peris J. Differential increase in taurine levels by low-dose ethanol in the dorsal and ventral striatum revealed by microdialysis with on-line capillary electrophoresis. Alcohol. Clin. Exp. Res. 2004, 28:1028-1038.
72. Sobie E.A., Guatimosim S., Gomez-Viquez L., Song L.S., Hartmann H., Saleet Jafri M., Lederer W.J. The Ca 2+ leak paradox and rogue ryanodine receptors: SR Ca 2+ efflux theory and practice. Prog. Biophys. Mol. Biol. 2006, 90:172-185.
73. Sudhof T.C. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 1995, 375:645-653.
74. Sudhof T.C. The synaptic vesicle cycle. Annu. Rev. Neurosci. 2004, 27:509-547.
75. Sutton U., Simmonds M.A. Effects of acute and chronic ethanol on the gamma-amino-butyric acid system in rat brain. Biochem. Pharmacol. 1973, 22:1685-1692.
76. Tabakoff B., Nelson E., Yoshimura M., Hellevuo K., Hoffman P.L. Phosphorylation cascades control the actions of ethanol on cell cAMP signalling. J. Biomed. Sci. 2001, 8:44-51.
77. Talani G., Lovinger D. Ethanol and endocannabinoid interactions in the control of GABA release in rat basolateral amygdala. Abstract. Alcohol. Clin. Exp. Res. 2008, 32. #808.
78. Tan K.R., Brown M., Labouebe G., Yvon C., Creton C., Fritschy J.M., Rudolph U., Luscher C. Neural bases for addictive properties of benzodiazepines. Nature 2010, 463:769-774.
79. Theile J.W., Morikawa H., Gonzales R.A., Morrisett R.A. Ethanol enhances GABAergic transmission onto dopamine neurons in the ventral tegmental area of the rat. Alcohol. Clin. Exp. Res. 2008, 32:1040-1048.
80. Theile J.W., Morikawa H., Gonzales R.A., Morrisett R.A. Role of 5-hydroxytryptamine2C receptors in Ca2+-dependent ethanol potentiation of GABA release onto ventral tegmental area dopamine neurons. J. Pharmacol. Exp. Ther. 2009, 329:625-633.
81. Veinante P., Stoeckel M.E., Freund-Mercier M.J. GABA- and peptide-immunoreactivities co-localize in the rat central extended amygdala. NeuroReport 1997, 8:2985-2989.
82. Volicer L., Klosowicz B.A. Effect of ethanol and stress on gamma-aminobutyric acid and guanosine 3', 5'-monophosphate levels in the rat brain. Biochem. Pharmacol. 1979, 28:2677-2679.
83. Volpicelli J.R., Watson N.T., King A.C., Sherman C.E., O'Brien C.P. Effect of naltrexone on alcohol "high" in alcoholics. Am. J. Psychiatry 1995, 152:613-615.
84. Wan F.J., Berton F., Madamba S.G., Francesconi W., 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. USA 1996, 93:5049-5054.
85. Ward R.J., Colivicchi M.A., Allen R., Schol F., Lallemand F., de Witte P., Ballini C., Corte L.D., Dexter D. Neuro-inflammation induced in the hippocampus of 'binge drinking' rats may be mediated by elevated extracellular glutamate content. J. Neurochem. 2009, 111:1119-1128.
86. Weiner J.L., Valenzuela C.F. Ethanol modulation of GABAergic transmission: the view from the slice. Pharmacol. Ther. 2006, 111:533-554.
87. Wills T.A., Knapp D.J., Overstreet D.H., Breese G.R. Sensitization, duration, and pharmacological blockade of anxiety-like behavior following repeated ethanol withdrawal in adolescent and adult rats. Alcohol. Clin. Exp. Res. 2009, 33:455-463.
88. Xiao C., Ye J.H. Ethanol dually modulates GABAergic synaptic transmission onto dopaminergic neurons in ventral tegmental area: role of mu-opioid receptors. Neuroscience 2008, 153:240-248.
89. Yamasaki M., Hashimoto K., Kano M. Miniature synaptic events elicited by presynaptic Ca2+ rise are selectively suppressed by cannabinoid receptor activation in cerebellar Purkinje cells. J. Neurosci. 2006, 26:86-95.
90. Yao L., Fan P., Jiang Z., Gordon A., Mochly-Rosen D., Diamond I. Dopamine and ethanol cause translocation of epsilonPKC associated with epsilonRACK: cross-talk between cAMP-dependent protein kinase A and protein kinase C signaling pathways. Mol. Pharmacol. 2008, 73:1105-1112.
91. Yoshimura M., Pearson S., Kadota Y., Gonzalez C.E. Identification of ethanol responsive domains of adenylyl cyclase. Alcohol. Clin. Exp. Res. 2006, 30:1824-1832.
92. Zhu P.J., Lovinger D.M. Ethanol potentiates GABAergic synaptic transmission in a postsynaptic neuron/synaptic bouton preparation from basolateral amygdala. J. Neurophysiol. 2006, 96:433-441.
93. Ziskind-Conhaim L., Gao B.X., Hinckley C. Ethanol dual modulatory actions on spontaneous postsynaptic currents in spinal motoneurons. J. Neurophysiol. 2003, 89:806-813.
94. Zucker R.S. Short-term synaptic plasticity. Annu. Rev. Neurosci. 1989, 12:13-31.
95. Zuo G.C., Yang J.Y., Hao Y., Dong Y.X., Wu C.F. Ethanol and acetaldehyde induce similar changes in extracellular levels of glutamate, taurine and GABA in rat anterior cingulate cortex. Toxicol. Lett. 2007, 169:253-258.