Cell-type-specific tonic GABA signaling in the rat central amygdala is selectively altered by acute and chronic ethanol

Addiction Biology

Volumn 21, Issue 1, 2016, Pages 72-86

  Herman, Melissa Ann ^a   Roberto, Marisa ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Alcohol; delta; GABAA

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ALCOHOL; CENTRAL DEPRESSANT AGENT; GABRA1 PROTEIN, RAT; GABRD PROTEIN, RAT;

ADULT; ALCOHOL ABUSE; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE CONDUCTANCE; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; CURRENT CLAMP TECHNIQUE; ELECTROPHYSIOLOGY; ENVIRONMENTAL EXPOSURE; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE CURRENT; MEMBRANE DEPOLARIZATION; NERVE EXCITABILITY; NEUROTRANSMISSION; NONHUMAN; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; RAT; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; WHOLE CELL PATCH CLAMP; ANIMAL; DRUG EFFECTS; METABOLISM; NERVE CELL; PATCH CLAMP TECHNIQUE;

ANIMALS; CENTRAL AMYGDALOID NUCLEUS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; GAMMA-AMINOBUTYRIC ACID; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RECEPTORS, GABA-A;

EID: 84957672901     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/adb.12181     Document Type: Article

References (40)

1. Ade KK, Janssen MJ, Ortinski PI, Vicini S, (2008) Differential tonic GABA conductances in striatal medium spiny neurons. J Neurosci 28: 1185-1197.
2. Alheid GF, Heimer L, (1988) New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27: 1-39.
3. Baur R, Kaur KH, Sigel E, (2009) Structure of alpha6 beta3 delta GABA(A) receptors and their lack of ethanol sensitivity. J Neurochem 111: 1172-1181.
4. Belelli D, Harrison NL, Maguire J, Macdonald RL, Walker MC, Cope DW, (2009) Extrasynaptic GABAA receptors: form, pharmacology, and function. J Neurosci 29: 12757-12763.
5. Borghese CM, Harris RA, (2007) Studies of ethanol actions on recombinant delta-containing gamma-aminobutyric acid type A receptors yield contradictory results. Alcohol 41: 155-162.
6. Botta P, Radcliffe RA, Carta M, Mameli M, Daly E, Floyd KL, Deitrich RA, Valenzuela CF, (2007) Modulation of GABAA receptors in cerebellar granule neurons by ethanol: a review of genetic and electrophysiological studies. Alcohol 41: 187-199.
7. Bright DP, Renzi M, Bartram J, McGee TP, MacKenzie G, Hosie AM, Farrant M, Brickley SG, (2011) Profound desensitization by ambient GABA limits activation of delta-containing GABAA receptors during spillover. J Neurosci 31: 753-763.
8. Caraiscos VB, Elliott EM, You-Ten KE, Cheng VY, Belelli D, Newell JG, Jackson MF, Lambert JJ, Rosahl TW, Wafford KA, MacDonald JF, Orser BA, (2004) Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by alpha5 subunit-containing gamma-aminobutyric acid type A receptors. Proc Natl Acad Sci U S A 101: 3662-3667.
9. Carta M, Mameli M, Valenzuela CF, (2004) Alcohol enhances GABAergic transmission to cerebellar granule cells via an increase in Golgi cell excitability. J Neurosci 24: 3746-3751.
10. Chieng BC, Christie MJ, Osborne PB, (2006) Characterization of neurons in the rat central nucleus of the amygdala: cellular physiology, morphology, and opioid sensitivity. J Comp Neurol 497: 910-927.
11. Drasbek KR, Jensen K, (2006) THIP, a hypnotic and antinociceptive drug, enhances an extrasynaptic GABAA receptor-mediated conductance in mouse neocortex. Cereb Cortex 16: 1134-1141.
12. Dumont EC, Martina M, Samson RD, Drolet G, Pare D, (2002) Physiological properties of central amygdala neurons: species differences. Eur J Neurosci 15: 545-552.
13. Gilpin NW, Roberto M, (2012) Neuropeptide modulation of central amygdala neuroplasticity is a key mediator of alcohol dependence. Neurosci Biobehav Rev 36: 873-888.
14. Glykys J, Mody I, (2007a) Activation of GABAA receptors: views from outside the synaptic cleft. Neuron 56: 763-770.
15. Glykys J, Mody I, (2007b) The main source of ambient GABA responsible for tonic inhibition in the mouse hippocampus. J Physiol 582: 1163-1178.
16. Glykys J, Peng Z, Chandra D, Homanics GE, Houser CR, Mody I, (2007) A new naturally occurring GABA(A) receptor subunit partnership with high sensitivity to ethanol. Nat Neurosci 10: 40-48.
17. Hanchar HJ, Dodson PD, Olsen RW, Otis TS, Wallner M, (2005) Alcohol-induced motor impairment caused by increased extrasynaptic GABA(A) receptor activity. Nat Neurosci 8: 339-345.
18. Herman MA, Contet C, Justice NJ, Vale W, Roberto M, (2013) Novel subunit-specific tonic GABA currents and differential effects of ethanol in the central amygdala of CRF receptor-1 reporter mice. J Neurosci 33: 3284-3298.
19. Hyytia P, Koob GF, (1995) GABAA receptor antagonism in the extended amygdala decreases ethanol self-administration in rats. Eur J Pharmacol 283: 151-159.
20. Jia F, Chandra D, Homanics GE, Harrison NL, (2008) Ethanol modulates synaptic and extrasynaptic GABAA receptors in the thalamus. J Pharmacol Exp Ther 326: 475-482.
21. Krook-Magnuson EI, Huntsman MM, (2005) Excitability of cortical neurons depends upon a powerful tonic conductance in inhibitory networks. Thalamus Relat Syst 3: 115-120.
22. Liang J, Suryanarayanan A, Abriam A, Snyder B, Olsen RW, Spigelman I, (2007) Mechanisms of reversible GABAA receptor plasticity after ethanol intoxication. J Neurosci 27: 12367-12377.
23. Marowsky A, Rudolph U, Fritschy JM, Arand M, (2012) Tonic inhibition in principal cells of the amygdala: a central role for alpha3 subunit-containing GABAA receptors. J Neurosci 32: 8611-8619.
24. Mhatre MC, Ticku MK, (1992) Chronic ethanol administration alters gamma-aminobutyric acidA receptor gene expression. Mol Pharmacol 42: 415-422.
25. Mitchell EA, Gentet LJ, Dempster J, Belelli D, (2007) GABAA and glycine receptor-mediated transmission in rat lamina II neurones: relevance to the analgesic actions of neuroactive steroids. J Physiol 583: 1021-1040.
26. Morrow AL, Herbert JS, Montpied P, (1992) Differential effects of chronic ethanol administration on GABA(A) receptor alpha1 and alpha6 subunit mRNA levels in rat cerebellum. Mol Cell Neurosci 3: 251-258.
27. Nusser Z, Sieghart W, Somogyi P, (1998) Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 18: 1693-1703.
28. O'Dell LE, Roberts AJ, Smith RT, Koob GF, (2004) Enhanced alcohol self-administration after intermittent versus continuous alcohol vapor exposure. Alcohol Clin Exp Res 28: 1676-1682.
29. Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G, (2000) GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101: 815-850.
30. Pitkanen A, Amaral DG, (1994) The distribution of GABAergic cells, fibers, and terminals in the monkey amygdaloid complex: an immunohistochemical and in situ hybridization study. J Neurosci 14: 2200-2224.
31. Roberto M, Madamba SG, Moore SD, Tallent MK, Siggins GR, (2003) Ethanol increases GABAergic transmission at both pre- and postsynaptic sites in rat central amygdala neurons. Proc Natl Acad Sci U S A 100: 2053-2058.
32. Roberto M, Madamba SG, Stouffer DG, Parsons LH, Siggins GR, (2004) Increased GABA release in the central amygdala of ethanol-dependent rats. J Neurosci 24: 10159-10166.
33. Roberts AJ, Cole M, Koob GF, (1996) Intra-amygdala muscimol decreases operant ethanol self-administration in dependent rats. Alcohol Clin Exp Res 20: 1289-1298.
34. Sanger DJ, Morel E, Perrault G, (1996) Comparison of the pharmacological profiles of the hypnotic drugs, zaleplon and zolpidem. Eur J Pharmacol 313: 35-42.
35. Semyanov A, Walker MC, Kullmann DM, Silver RA, (2004) Tonically active GABA A receptors: modulating gain and maintaining the tone. Trends Neurosci 27: 262-269.
36. Stell BM, Brickley SG, Tang CY, Farrant M, Mody I, (2003) Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by delta subunit-containing GABAA receptors. Proc Natl Acad Sci U S A 100: 14439-14444.
37. Sur C, Farrar SJ, Kerby J, Whiting PJ, Atack JR, McKernan RM, (1999) Preferential coassembly of alpha4 and delta subunits of the gamma-aminobutyric acid A receptor in rat thalamus. Mol Pharmacol 56: 110-115.
38. Veinante P, Freund-Mercier MJ, (1998) Intrinsic and extrinsic connections of the rat central extended amygdala: an in vivo electrophysiological study of the central amygdaloid nucleus. Brain Res 794: 188-198.
39. Wallner M, Hanchar HJ, Olsen RW, (2003) Ethanol enhances alpha 4 beta 3 delta and alpha 6 beta 3 delta gamma-aminobutyric acid type A receptors at low concentrations known to affect humans. Proc Natl Acad Sci U S A 100: 15218-15223.
40. Wei W, Faria LC, Mody I, (2004) Low ethanol concentrations selectively augment the tonic inhibition mediated by delta subunit-containing GABAA receptors in hippocampal neurons. J Neurosci 24: 8379-8382.