Specific subtypes of GABAA receptors mediate phasic and tonic forms of inhibition in hippocampal pyramidal neurons

Journal of Neurophysiology

Volumn 96, Issue 2, 2006, Pages 846-857

  Prenosil, George A ^a   Gasser, Edith M Schneider ^a   Rudolph, Uwe ^a   Keist, Ruth ^a   Fritschy, Jean Marc ^a   Vogt, Kaspar E ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; DIAZEPAM; RECEPTOR SUBUNIT; SLOW ADAPTING RECEPTOR; SYNAPSE RECEPTOR; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; GABRA1 PROTEIN, MOUSE; GABRA2 PROTEIN, MOUSE; HYPNOTIC SEDATIVE AGENT; PHOSPHINIC ACID DERIVATIVE; PROPANOLAMINE DERIVATIVE; PROTEIN SUBUNIT;

4 AMINOBUTYRIC ACID UPTAKE; ALPHA CHAIN; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EVOKED RESPONSE; HIPPOCAMPUS; INHIBITION KINETICS; MOUSE; NONHUMAN; PATCH CLAMP; POINT MUTATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SENSITIVITY ANALYSIS; ANIMAL; CYTOLOGY; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; GENOTYPE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; STATISTICAL ANALYSIS; TRANSGENIC MOUSE;

ANIMALS; DATA INTERPRETATION, STATISTICAL; DIAZEPAM; ELECTROPHYSIOLOGY; EVOKED POTENTIALS; EXCITATORY POSTSYNAPTIC POTENTIALS; GENOTYPE; HIPPOCAMPUS; HYPNOTICS AND SEDATIVES; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; PATCH-CLAMP TECHNIQUES; PHOSPHINIC ACIDS; POINT MUTATION; PROPANOLAMINES; PROTEIN SUBUNITS; PYRAMIDAL CELLS; RECEPTORS, GABA-A;

EID: 33746630203     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01199.2006     Document Type: Article

References (71)

1. Bacci A, Rudolph U, Huguenard JR, and Prince DA. Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses. J Neurosci 23: 9664-9674, 2003.
2. A receptor-mediated inhibitory postsynaptic currents in hippocampus. J Neurophysiol 88: 3097-3107, 2002.
3. A,slow. J Neurosci 18: 1305-1317, 1998.
4. A receptors in CA1 pyramidal cells. J Neurosci 20: 937-948, 2000.
5. A circuits in hippocampus. Neuron 25: 449-457, 2000.
6. A receptors: classification on the basis of subunit structure and receptor function. Pharmacol Rev 50: 291-313, 1998.
7. A receptors containing two different types of α subunits in murine brain using point-mutated α subunits. J Biol Chem 279: 43654-43660, 2004.
8. A receptors rendered diazepam-insensitive by point-mutated α-subunits. FEBS Lett 431: 400-404, 1998.
9. A receptor subtype have normal number of synapses, but retain juvenile IPSC kinetics until adulthood. J Neurophysiol 94: 338-346, 2005.
10. A receptor α subunits. J Physiol 545: 169-181, 2002.
11. A receptors. J Physiol 497: 753-759, 1996.
12. Brunig I, Scotti E, Sidler C, and Fritschy JM. Intact sorting, targeting, and clustering of γ-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J Comp Neurol 443: 43-55, 2002.
13. Caraiscos VB, Elliott EM, You-Ten KE, Cheng VY, Belelli D, Newell JG, Jackson MF, Lambert JJ, Rosahl TW, Wafford KA, MacDonald JF, and Orser BA. Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by α5 subunit-containing γ-aminobutyric acid type A receptors. Proc Natl Acad Sci USA 101: 3662-3667, 2004a.
14. Caraiscos VB, Newell JG, You-Ten KE, Elliott EM, Rosahl TW, Wafford KA, MacDonald JF, and 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.
15. A receptor-mediated tonic inhibition in thalamic neurons. J Neurosci 25: 11553-11563, 2005.
16. A receptors. Proc Natl Acad Sci USA 99: 8980-8985, 2002.
17. A receptor-mediated conductance in mouse neocortex. Cereb Cortex Oct 2005; 10.1093/ceicol/bhj055.
18. A circuits for visual cortical plasticity. Science 303: 1681-1683, 2004.
19. A receptors. Nat Rev Neurosci 6: 215-229, 2005.
20. Freund TF and Buzsaki G. Interneurons of the hippocampus. Hippocampus 6: 347-470, 1996.
21. A-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359: 154-194, 1995.
22. A receptor subunits revealed by antigen-retrieval immunohistochemistry. J Comp Neurol 390: 194-210, 1998.
23. A receptor α5 subunit deficient mice. J Neurophysiol Feb 1, 2006; 10.1152/jn. 01122.2005.
24. A receptor α1 subunit. J Neurophysiol 88: 3208-3217, 2002.
25. A receptor occupancy. Eur J Neurosci 12: 810-818, 2000.
26. A receptor α-subunit clustering in the developing rat neocortex and hippocampus. Eur J Neurosci 19: 2475-2487, 2004.
27. A receptor desensitization kinetics and its role in synapse function in rat cortical neurons. J Physiol 522: 3-17, 2000.
28. Klausberger T. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421: 844-848, 2003.
29. A receptors in the hippocampus. J Neurosci 22: 2513-2521, 2002.
30. A-receptor confers sensitivity to benzodiazepine receptor ligands. FEBS Lett 293: 191-194, 1991.
31. A receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 12: 4151-4172, 1992.
32. B autoreceptors. J Physiol 502: 91-104, 1997.
33. Low K, Crestani F, Keist R, Benke D, Brunig I, Benson JA, Fritschy JM, Rulicke T, Bluethmann H, Mohler H, and Rudolph U. Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290: 131-134, 2000.
34. A receptor subtypes in the amygdala. Eur J Neurosci 20: 1281-1289, 2004.
35. A receptors. J Physiol 515: 711-727, 1999.
36. A receptor α1 subtype. Nat Neurosci 3: 587-592, 2000.
37. A-receptor subtypes really occur in the brain? Trends Neurosci 19: 139-143, 1996.
38. A receptors. Trends Neurosci 27: 569-575, 2004.
39. A circuits in brain development and therapy. Biochem Pharmacol 68: 1685-1690, 2004.
40. Mohler H, Fritschy JM, and Rudolph U. A new benzodiazepine pharmacology. J Pharmacol Exp Ther 300: 2-8, 2002.
41. A receptors mediate tonic inhibition in hippocampal dentate granule cells. Mol Pharmacol 69: 564-575, 2006.
42. Nusser Z and Mody I. Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol 87: 2624-2628, 2002.
43. Nusser Z, Sieghart W, Benke D, Fritschy JM, and Somogyi P. Differential synaptic localization of two major γ-aminobutyric acid type A receptor α subunits on hippocampal pyramidal cells. Proc Natl Acad Sci USA 93: 11939-11944, 1996.
44. A receptors in synapses of hippocampal pyramidal cells of the rat. Eur J Neurosci 13: 428-442, 2001.
45. A responses in rat hippocampus. Neuron 10: 189-200, 1993.
46. A receptors in central synapses. J Neurosci 19: 578-588, 1999.
47. Perrais D and Ropert N. Altering the concentration of GABA in the synaptic cleft potentiates miniature IPSCs in rat occipital cortex. Eur J Neurosci 12: 400-404, 2000.
48. A receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101: 815-850, 2000.
49. Porcello DM, Huntsman MM, Mihalek RM, Homanics GE, and Huguenard JR. Intact synaptic GABAergic inhibition and altered neurosteroid modulation of thalamic relay neurons in mice lacking δ subunit. J Neurophysiol 89: 1378-1386, 2003.
50. Pouille F and Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293: 1159-1163, 2001.
51. Pouille F and Scanziani M. Routing of spike series by dynamic circuits in the hippocampus. Nature 429: 717-723, 2004.
52. Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, and Capogna M. Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25: 6775-6786, 2005.
53. A receptor subunit for benzodiazepine pharmacology. Nature 338: 582-585, 1989.
54. A receptors which contain the alpha 5 subunit. Neuropharmacology 35: 1331-1335, 1996.
55. A receptor subtypes. Nature 401: 796-800, 1999.
56. A receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu Rev Pharmacol Toxicol 44: 475-498, 2004.
57. B receptors to control rhythmic hippocampal activity. Neuron 25: 673-681, 2000.
58. A receptors containing α4β3γ2, α4γ2, or α1β3γ2 subunits. Eur J Pharmacol 304: 155-162, 1996.
59. A receptor currents in the hippocampus. J Neurosci 25: 10016-10024, 2005.
60. Semyanov A, Walker MC, and Kullmann DM. GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6: 484-490, 2003.
61. A receptors: modulating gain and maintaining the tone. Trends Neurosci 27: 262-269, 2004.
62. A receptor subtypes. Curr Top Med Chem 2: 795-816, 2002.
63. 36Cl ion flux. Mol Pharmacol 59: 1108-1118, 2001.
64. A receptors. Proc Natl Acad Sci USA 100: 14439-14444, 2003.
65. A receptors in hippocampal granule cells. Brain Res 1029: 207-216, 2004.
66. Thomson AM, Bannister AP, Hughes DI, and Pawelzik H. Differential sensitivity to Zolpidem of IPSPs activated by morphologically identified CA1 interneurons in slices of rat hippocampus. Eur J Neurosci 12: 425-436, 2000.
67. A receptors affect the dynamic range of mouse hippocampal kainate-induced gamma frequency oscillations in vitro. J Physiol 559: 721-728, 2004.
68. A receptor α1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J Neurosci 21: 3009-3016, 2001.
69. A) kinetics provide substrate for mixed gamma-theta rhythm. Proc Natl Acad Sci USA 97: 8128-8133, 2000.
70. A receptors is essential for benzodiazepine agonist binding. J Biol Chem 267: 1426-1429, 1992.
71. Yee BK, Hauser J, Dolgov VV, Keist R, Mohler H, Rudolph U, and Feldon J. GABA receptors containing the α5 subunit mediate the trace effect in aversive and appetitive conditioning and extinction of conditioned fear. Eur J Neurosci 20: 1928-1936, 2004.