α5GABAA receptors regulate the intrinsic excitability of mouse hippocampal pyramidal neurons

Journal of Neurophysiology

Volumn 98, Issue 4, 2007, Pages 2244-2254

  Bonin, Robert P ^a   Martin, Loren J ^a   MacDonald, John F ^a   Orser, Beverley A ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b SUNNYBROOK RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; AMINO ACID RECEPTOR BLOCKING AGENT; AMINO ACID RECEPTOR STIMULATING AGENT; GABRA5 PROTEIN, MOUSE; IMIDAZOLE DERIVATIVE; L 655,708; PICROTOXIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; HIPPOCAMPUS; HYPERPOLARIZATION; MEMBRANE POTENTIAL; MOUSE; NERVE CELL; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MEMBRANE POTENTIAL; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; MOUSE MUTANT; PATCH CLAMP; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; CELLS, CULTURED; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; IMIDAZOLES; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PATCH-CLAMP TECHNIQUES; PICROTOXIN; PYRAMIDAL CELLS; RECEPTORS, GABA-A;

EID: 35348838988     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00482.2007     Document Type: Article

References (61)

1. Attwell D, Barbour B, Szatkowski M. Nonvesicular release of neurotransmitter. Neuron 11: 401-407, 1993.
2. Bai D, Zhu G, Pennefather P, Jackson MF, MacDonald JF, Orser BA. Distinct functional and pharmacological properties of tonic and quantal inhibitory postsynaptic currents mediated by gamma-aminobutyric acid(A) receptors in hippocampal neurons. Mol Pharmacol 59: 814-824, 2001.
3. A receptors. J Physiol 497: 753-759, 1996.
4. Brickley SG, Revilla V, Cull-Candy SG, Wisden W, Farrant M. Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409: 88-92, 2001.
5. Brunig I, Scotti E, Sidler C, Fritschy JM. Intact sorting, targeting, and clustering of gamma-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J Comp Neurol 443: 43-55, 2002.
6. Caraiscos VB, Elliott EM, You T, Cheng VY, Belelli D, Newell JG, Jackson MF, Lambert JJ, Rosahl TW, Wafford KA, MacDonald JF, Orser BA. Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by {alpha}5 subunit-containing {gamma}-aminobutyric acid type A receptors. Proc Natl Acad Sci USA 101: 3662-3667, 2004a.
7. Caraiscos VB, Newell JG, You T, Elliott EM, Rosahl TW, Wafford KA, MacDonald JF, Orser BA. Selective enhancement of tonic GABAergic inhibition in murine hippocampal neurons by low concentrations of the volatile anesthetic isoflurane. J Neurosci 24: 8454-8458, 2004b.
8. Chambers MS, Atack JR, Broughton HB, Collinson N, Cook S, Dawson GR, Hobbs SC, Marshall G, Maubach KA, Pillai GV, Reeve AJ, MacLeod AM. Identification of a novel, selective GABA(A) alpha5 receptor inverse agonist which enhances cognition. J Med Chem 46: 2227-2240, 2003.
9. Chance FS, Abbott LF, Reyes AD. Gain modulation from background synaptic input. Neuron 35: 773-782, 2002.
10. A receptors mediate the amnestic but not sedative-hypnotic effects of the general anesthetic etomidate. J Neurosci 26: 3713-3720, 2006.
11. A receptor clustering in cultured hippocampal neurons. J Neurosci 22: 684-697, 2002.
12. Cobb SR, Burl EH, Halasy K, Paulsen O, Somogyi P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378: 75-78, 1995.
13. A receptor. J Neurosci 22: 5572-5580, 2002.
14. Crestani F, Keist R, Fritschy JM, Benke D, Vogt K, Prut L, Bluthmann H, Mohler H, Rudolph U. Trace fear conditioning involves hippocampal alpha5 GABA(A) receptors. Proc Natl Acad Sci USA 99: 8980-8985, 2002.
15. Csicsvari J, Jamieson B, Wise KD, Buzsaki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37: 311-322, 2003.
16. Curmi JP, Premkumar LS, Birnir B, Gage PW. The influence of membrane potential on chloride channels activated by GABA in rat cultured hippocampal neurons. J Membr Biol 136: 273-280, 1993.
17. Dawson GR, Maubach KA, Collinson N, Cobain M, Everitt BJ, MacLeod AM, Choudhury HI, McDonald LM, Pillai G, Rycroft W, Smith AJ, Sternfeld F, Tattersall FD, Wafford KA, Reynolds DS, Seabrook GR, Atack JR. An inverse agonist selective for {alpha}5 subunit-containing GABAA receptors enhances cognition. J Pharmacol Exp Ther 316: 1335-1345, 2006.
18. A-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359: 54-94, 1995.
19. Glykys J, Mody I. Hippocampal network hyperactivity following selective reduction of tonic inhibition in GABAA receptor {alpha}5 subunit deficient mice. J Neurophysiol 95: 2796-2807, 2006.
20. Hamann M, Rossi DJ, Attwell D. Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33: 625-633, 2002.
21. Jones A, Korpi ER, McKernan RM, Pelz R, Nusser Z, Makela R, Mellor JR, Pollard S, Bahn S, Stephenson FA, Randall AD, Sieghart W, Somogyi P, Smith AJ, Wisden W. Ligand-gated ion channel subunit partnerships: GABAA receptor alpha6 subunit gene inactivation inhibits delta subunit expression. J Neurosci 17: 1350-1362, 1997.
22. Khirug S, Huttu K, Ludwig A, Smirnov S, Voipio J, Rivera C, Kaila K, Khiroug L. Distinct properties of functional KCC2 expression in immature mouse hippocampal neurons in culture and in acute slices. Eur J Neurosci 21: 899-904, 2005.
23. Kralic JE, Korpi ER, O'Buckley TK, Homanics GE, Morrow AL. Molecular and pharmacological characterization of GABA(A) receptor alpha1 subunit knockout mice. J Pharmacol Exp Ther 302: 1037-1045, 2002.
24. Kralic JE, Sidler C, Parpan F, Homanics GE, Morrow AL, Fritschy JM. Compensatory alteration of inhibitory synaptic circuits in cerebellum and thalamus of gamma-aminobutyric acid type A receptor alpha1 subunit knockout mice. J Comp Neurol 495: 408-421, 2006.
25. A receptors in the CNS: where and why? Prog Biophys Mol Biol 87: 33-46, 2005.
26. Lacaille JC, Mueller AL, Kunkel DD, Schwartzkroin PA. Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 7: 1979-1993, 1987.
27. Lerma J, Herranz AS, Herreras O, Abraira V, Martin DR. In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res 384: 145-155, 1986.
28. Lisman JE. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22: 233-242, 1999.
29. MacDonald JF, Mody I, Salter MW. Regulation of N-methyl-D-aspartate receptors revealed by intracellular dialysis of murine neurons in culture. J Physiol 414: 17-34, 1989.
30. Maguire JL, Stell BM, Rafizadeh M, Mody I. Ovarian cycle-linked changes in GABA(A) receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat Neurosci 8: 797-804, 2005.
31. A-mediated conductance selectively enhances the glutamatergic drive of principal cells. J Physiol 581: 515-528, 2007.
32. A receptors in hippocampal pyramidal neurons exhibit constitutive GABA-independent gating. Mol Pharmacol 71: 539-548, 2007.
33. A-receptor subtypes really occur in the brain? Trends Neurosci 19: 139-143, 1996.
34. Mitchell SJ, Silver RA. Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38: 433-445, 2003.
35. Mody I. Distinguishing between GABA(A) receptors responsible for tonic and phasic conductances. Neurochem Res 26: 907-913, 2001.
36. Ortinski PI, Turner JR, Barberis A, Motamedi G, Yasuda RP, Wolfe BB, Kellar KJ, Vicini S. Deletion of the GABA(A) receptor alpha1 subunit increases tonic GABA(A) receptor current: a role for GABA uptake transporters. J Neurosci 26: 9323-9331, 2006.
37. Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G. GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101: 815-850, 2000.
38. A receptors mediate phasic and tonic forms of inhibition in hippocampal pyramidal neurons. J Neurophysiol 96: 846-857, 2006.
39. +/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397: 251-255, 1999.
40. Rossi DJ, Hamman M, Attwell D. Multiple modes of GABAergic inhibition of rat cerebellar granule cells. J Physiol 548: 97-110, 2003.
41. Rudolph U, Crestani F, Mohler H. GABA(A) receptor subtypes: dissecting their pharmacological functions. Trends Pharmacol Sci 22: 188-194, 2001.
42. Sassoe-Pognetto M, Panzanelli P, Sieghart W, Fritschy JM. Colocalization of multiple GABA(A) receptor subtypes with gephyrin at postsynaptic sites. J Comp Neurol 420: 481-498, 2000.
43. Scanziani M. GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity. Neuron 25: 673-681, 2000.
44. A receptor currents in the hippocampus. J Neurosci 25: 10016-10024, 2005.
45. Semyanov A, Walker MC, Kullmann DM. GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6: 484-490, 2003.
46. A receptors: modulating gain and maintaining the tone. Trends Neurosci 27: 262-269, 2004.
47. A receptors containing the alpha5 subunit in the rat brain. J Comp Neurol 499: 458-470, 2006.
48. Stell BM, Brickley SG, Tang CY, Farrant M, Mody I. Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by {delta} subunit-containing GABAA receptors. Proc Natl Acad Sci USA 100: 14439-14444, 2003.
49. A conductances in hippocampal neurons. J Neurosci 22: 1-5, 2002.
50. Sternfeld F, Carling RW, Jelley RA, Ladduwahetty T, Merchant KJ, Moore KW, Reeve AJ, Street LJ, O'Connor D, Sohal B, Atack JR, Cook S, Seabrook G, Wafford K, Tattersall FD, Collinson N, Dawson GR, Castro JL, MacLeod AM. Selective, orally active gamma-aminobutyric acidA alpha5 receptor inverse agonists as cognition enhancers. J Med Chem 47: 2176-2179, 2004.
51. Sur C, Fresu L, Howell O, McKernan RM, Atack JR. Autoradiographic localization of alpha5 subunit-containing GABAA receptors in rat brain. Brain Res 822: 265-270, 1999.
52. Tossman U, Jonsson G, Ungerstedt U. Regional distribution and extracellular levels of amino acids in rat central nervous system. Acta Physiol Scand 127: 533-545, 1986.
53. A receptors affect the dynamic range of mouse hippocampal kainate-induced gamma frequency oscillations in vitro. J Physiol 559: 721-728, 2004.
54. - channels are randomly activated by continuous GABA secretion in cultured embryonic rat hippocampal neurons. Neurosci Lett 155: 199-203, 1993.
55. Vautrin J, Maric D, Sukhareva M, Schaffner AE, Barker JL. Surface-accessible GABA supports tonic and quantal synaptic transmission. Synapse 37: 38-55, 2000.
56. Wall MJ, Usowicz MM. Development of the quantal properties of evoked and spontaneous synaptic currents at a brain synapse. Nat Neurosci 1: 675-682, 1998.
57. Whiting PJ, Bonnert TP, McKernan RM, Farrar S, Le Bourdelles B, Heavens RP, Smith DW, Hewson L, Rigby MR, Sirinathsinghji DJ, Thompson SA, Wafford KA. Molecular and functional diversity of the expanding GABA-A receptor gene family. Ann NY Acad Sci 868: 645-653, 1999.
58. Whittington MA, Jefferys JG, Traub RD. Effects of intravenous anaesthetic agents on fast inhibitory oscillations in the rat hippocampus in vitro. Br J Pharmacol 118: 1977-1986, 1996.
59. Wisden W, Laurie DJ, Monyer H, Seeburg PH. The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 12: 1040-1062, 1992.
60. Woodin MA, Ganguly K, Poo MM. Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl- transporter activity. Neuron 39: 807-820, 2003.
61. A receptors in hippocampal neurons are high-affinity, low-conductance sensors for extracellular GABA. Mol Pharm 63: 2-8, 2003.