Aspects of the homeostaic plasticity of GABAA receptor-mediated inhibition

Journal of Physiology

Volumn 562, Issue 1, 2005, Pages 37-46

  Mody, Istvan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; EXCITATORY AMINO ACID; ION CHANNEL; AMINO ACID; CALCIUM CHANNEL; NEUROTRANSMITTER; PROTEIN KINASE B;

CELL FUNCTION; CELL METABOLISM; LEARNING; MEMORY; NERVE CELL INHIBITION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR BLOCKING; REVIEW; ARTICLE; CENTRAL NERVOUS SYSTEM; CHANNEL GATING; HOMEOSTASIS; MOUSE; NERVE CELL; SYNAPTIC TRANSMISSION;

ANIMALS; HOMEOSTASIS; HUMANS; ION CHANNEL GATING; NEURONAL PLASTICITY; NEURONS; RECEPTORS, GABA-A;

EID: 13444274766     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2004.077362     Document Type: Review

References (110)

1. Abbott LF & Nelson SB (2000). Synaptic plasticity: taming the beast. Nat Neurosci 3 (suppl.), 1178-1183.
2. Adkins JC & Noble S (1998). Tiagabine. A review of its pharmacodynamic and pharmacokinetic properties and therapeutic potential in the management of epilepsy. Drugs 55, 437-460.
3. A receptors characterized by fluorescence resonance energy transfer-derived measurements of membrane potential. J Biol Chem 276, 38934-38939.
4. Bacci A, Huguenard JR & Prince DA (2002). Differential modulation of synaptic transmission by neuropeptide Y in rat neocortical neurons. Proc Natl Acad Sci U S A 99, 17125-17130.
5. Bai D, Zhu G, Pennefather P, Jackson MF, MacDonald JF & Orser BA (2001). 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.
6. A receptor gamma 2 subunit in rat brain. Neuropharmacology 41, 745-752.
7. A receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway. J Biol Chem 275, 38856-38862.
8. Brandon N, Jovanovic J & Moss S (2002). Multiple roles of protein kinases in the modulation of gamma-aminobutyric acid (A) receptor function and cell surface expression. Pharmacol Ther 94, 113-122.
9. A receptors. J Physiol 497, 753-759.
10. Brickley SG, Revilla V, Cull-Candy SG, Wisden W & Farrant M (2001). Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409, 88-92.
11. A receptors. Br J Pharmacol 136, 965-974.
12. Brunig I, Scotti E, Sidler C & Fritschy JM (2002). Intact sorting, targeting, and clustering of gamma-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J Comp Neurol 443, 43-55.
13. Brunig I, Sommer M, Hatt H & Bormann J (1999). Dopamine receptor subtypes modulate olfactory bulb gamma-aminobutyric acid type A receptors. Proc Natl Acad Sci U S A 96, 2456-2460.
14. A-receptor function in the adult brain: insights from the oxytocin neurone. Trends Neurosci 23, 190-195.
15. Brussaard AB, Wossink J, Lodder JC & Kits KS (2000). Progesterone-metabolite prevents protein kinase C-dependent modulation of gamma-aminobutyric acid type A receptors in oxytocin neurons. Proc Natl Acad Sci U S A 97 3625-3630.
16. Buhl EH, Otis TS & Mody I (1996). Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science 271, 369-373.
17. Caraiscos VB, Elliott EM, You T, 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 α5 subunit-containing γ-aminobutyric acid type A receptors. Proc Natl Acad Sci U S A 101, 3662-3667.
18. Chadderton P, Margrie TW & Hausser M (2004). Integration of quanta in cerebellar granule cells during sensory processing. Nature 428, 856-860.
19. Chance FS, Abbott LF & Reyes AD (2002). Gain modulation from background synaptic input. Neuron 35, 773-782.
20. Cherubini E & Conti F (2001). Generating diversity at GABAergic synapses. Trends Neurosci 24, 155-162.
21. Cohen AS, Lin DD & Coulter DA (2000). Protracted postnatal development of inhibitory synaptic transmission in rat hippocampal area CA1 neurons. J Neurophysiol 84, 2465-2476.
22. Corpechot C, Young J, Calvel M, Wehrey C, Veltz JN, Touyer G, Mouren M, Prasad VV, Banner C & Sjovall J (1993). Neurosteroids: 3 alpha-hydroxy-5 alpha-pregnan-20-one and its precursors in the brain, plasma, and steroidogenic glands of male and female rats. Endocrinology 133, 1003-1009.
23. Coulter DA (2001). Epilepsy-associated plasticity in gamma-aminobutyric acid receptor expression, function, and inhibitory synaptic properties. Int Rev Neurobiol 45, 237-252.
24. Davis GW & Bezprozvanny I (2001). Maintaining the stability of neural function: a homeostatic hypothesis. Annu Rev Physiol 63, 847-869.
25. De Witte P, Pinto E, Ansseau M & Verbanck P (2003). Alcohol and withdrawal: from animal research to clinical issues. Neurosci Biobehav Rev 27, 189-197.
26. Desai NS, Rutherford LC & Turrigiano GG (1999). Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat Neurosci 2, 515-520.
27. During MJ, Ryder KM & Spencer DD (1995). Hippocampal GABA transporter function in temporal-lobe epilepsy. Nature 376, 174-177.
28. Fancsik A, Linn DM & Tasker JG (2000). Neurosteroid modulation of GABA IPSCs is phosphorylation dependent. J Neurosci 20, 3067-3075.
29. Freund TF & Buzsáki G (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
30. Fritschy JM & Brunig I (2003). Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol Ther 98, 299-323.
31. Gabbiani F, Midtgaard J & Knöpfel T (1994). Synaptic integration in a model of cerebellar granule cells. J Neurophysiol 72, 999-1009.
32. Gabbiana JL, Caillard O & Ben Ari Y (2002). Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. Trends Neurosci 25, 564-570.
33. Golowasch J, Casey M, Abbott LF & Marder E (1999). Network stability from activity-dependent regulation of neuronal conductances. Neural Comput 11, 1079-1096.
34. Hamann M, Rossi DJ & Attwell D (2002). Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33, 625-633.
35. Harris RA, Paylor R, Abeliovich A, Tonegawa S & Wehner JM (1995). Mutant mice lacking the gamma isoform of protein kinase C show decreased behavioral actions of ethanol and altered function of gamma-aminobutyrate type A receptors. Proc Natl Acad Sci U S A 92, 3658-3662.
36. A receptor modulators and alcohol in mice lacking PKCepsilon. Nat Neurosci 2, 997-1002.
37. Hodge CW, Raber J, Walter H, AM, Olive MF, Mehmert K, Morrow AL & Messing RO (2002). Decreased anxiety-like behavior, reduced stress hormones, and neurosteroid supersensitivity in mice lacking protein kinase Cepsilon. J Clin Invest 110, 1003-1010.
38. A receptor activation in granule cells of the early postnatal dentate gyrus. J Neurophysiol 80, 2340-2351.
39. B receptors in the hippocampus. J Neurophysiol 90, 2690-2701.
40. A receptor α6 subunit gene inactivation inhibits δ subunit expression. J Neurosci 17, 1350-1362.
41. A receptors clustered at neocortical synapses. J Neurosci 22, 1328-1337.
42. A receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition. Curr Opin Neurobiol 13, 341-347.
43. A receptors in supraoptic nucleus around parturition. J Neurosci 23, 788-797.
44. A receptors. Prog Neurobiol 67, 113-159.
45. Krogsgaard-Larsen P, Frolund B & Frydenvang K (2000). GABA uptake inhibitors. Design, molecular pharmacology and therapeutic aspects. Curr Pharm Des 6, 1193-1209.
46. A receptors by endogenous and synthetic neuroactive steroids. Brain Res Brain Res Rev 37, 68-80.
47. A receptors. Brain Res Mol Brain Res 52, 173-181.
48. A receptor. J Neurochem 60 1972-1975.
49. Lerma J, Herranz AS, Herreras O, Abraira V & Martin del To R (1986). 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.
50. Levitan IB (1999). Modulation of ion channels by protein phosphorylation. How the brain works. Adv Second Messenger Phosphoprotein Res 33, 3-22.
51. A receptor subtypes in human temporal lobe epilepsy. J Neurosci 20, 5401-5419.
52. Lu YM, Mansuy IM, Kandel ER & Roder J (2000). Calcineurin-mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP. Neuron 26, 197-205.
53. A receptor channels. Annu Rev Neurosci 17, 569-602.
54. A receptor. Mechanism of action and physiological significance. Prog Neurobiol 38, 379-395.
55. A receptor β subunits determine regulation by cAMP-dependent protein kinase. Nature Neuroscience 1, 23-28.
56. 2+/calmodulin type II-dependent protein kinase. Neuropharmacology 36, 1377-1385.
57. A-receptor subtypes really occur in the brain? Trends Neurosci 19, 139-143.
58. Mihalek RM, Banerjee PK, Korpi ER, Quinlan JJ, Firestone LL, Mi ZP, Lagenaur C, Tretter V, Sieghart W, Anagnostaras SG, Sage JR, Fanselow MS, Guidotti A, Spigelman I, Li Z, DeLorey TM, Olsen RW & Homanics GE (1999). Attenuated sensitivity to neuroactive steroids in gamma-aminobutyrate type A receptor delta subunit knockout mice. Proc Natl Acad Sci U S A 96, 12905-12910.
59. Mitchell SJ & Silver RA (2003). Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38, 433-445.
60. A receptors responsible for tonic and phasic conductances. Neurochem Res 26 907-913.
61. Mody I, De Koninck Y, Otis TS & Soltesz I (1994). Bridging the cleft at GABA synapses in the brain. Trends Neurosci 17, 517-525.
62. A receptors. Trends Neurosci 27 569-575.
63. A receptors by tyrosine phosphorylation. Nature 377, 344-348.
64. A receptors by cAMP-dependent protein phosphorylation. Science 257, 661-665.
65. A receptors underlies potentiation at hippocampal inhibitory synapses. Nature 395, 172-177.
66. Nusser Z & Mody I (2002). Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol 87, 2624-2628.
67. A receptors by cAMP-dependent protein kinase in mouse cerebellar and olfactory bulb neurones. J Physiol 521, 421-435.
68. A receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 18, 1693-1703.
69. O'Connell AW, Fox GB, Kjoller C, Gallagher HC, Murphy KJ, Kelly J & Regan CM (2001). Anti-ischemic and cognition-enhancing properties of NNC-711, a gamma-aminobutyric acid reuptake inhibitor. Eur J Pharmacol 424, 37-44.
70. A receptors. Adv Biochem Psychopharmacol 48, 57-74.
71. Pages KP & Ries RK (1998). Use of anticonvulsants in benzodiazepine withdrawal. Am J Addict 7, 198-204.
72. Patrylo PR, Spencer DD & Williamson A (2001). GABA uptake and heterotransport are impaired in the dentate gyrus of epileptic rats and humans with temporal lobe sclerosis. J Neurophysiol 85, 1533-1542.
73. Paul SM & Purdy RH (1992). Neuroactive steroids. FASEB J 6, 2311-2322.
74. A receptor in a mouse model of temporal lobe epilepsy. J Neurosci 24, 8629-8639.
75. A receptor function by PKA and PKC in adult hippocampal neurons. J Neurosci 19, 674-683.
76. Poolos NP, Migliore M & Johnston D (2002). Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites. Nat Ncurosci 5,0 767-774.
77. Porcu P, Sogliano C, Cinus M, Purdy RH, Biggio G & Concas A (2003). Nicotine-induced changes in cerebrocortical neuroactive steroids and plasma corticosterone concentrations in the rat. Pharmacol Biochem Behav 74, 683-690.
78. A receptor-mediated responses in protein kinase C gamma (PKC gamma) and PKC epsilon null mice. J Pharmacol Exp Ther 305, 264-270.
79. Purdy RH, Morrow AL, Moore PH Jr & Paul SM (1991). Stress-induced elevations of gamma-aminobutyric acid type A receptor-active steroids in the rat brain. Proc Natl Acad Sci U S A 88, 4553-4557.
80. A receptor function and seizure susceptibility. J Neurosci 22, 3795-3805.
81. Rossi DJ, Hamann M & Attwell D (2003). Multiple modes of GABAergic inhibition of rat cerebellar granule cells. J Physiol 548, 97-110.
82. Royer S & Pare D (2003). Conservation of total synaptic weight through balanced synaptic depression and potentiation. Nature 422, 518-522.
83. Rupprecht R (2003). Neuroactive steroids: mechanisms of action and neuropsychopharmacological properties. Psychoneuroendocrinology 28, 139-168.
84. A receptor isoforms. Mol Pharmacol 49, 567-579.
85. Semyanov A, Walker MC & Kullmann DM (2003). GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6, 484-490.
86. A receptors: modulating gain and maintaining the tone. Trends Neurosci 27, 262-269.
87. Serra M, Pisul MG, Dazzi L, Purdy RH & Biggio G (2002). Prevention of the stress-induced increase in the concentration of neuroactive steroids in rat brain by long-term administration of mirtazapine but not of fluoxetine. J Psychopharmacol 16, 133-138.
88. A receptor subtypes. Curr Top Med Chem 2, 795-816.
89. Smith SS (2001). Pre-menstrual steroids. Cell Mol Life Sci 58, 1263-1275.
90. A receptor α4 subunit suppression prevents withdrawal properties of an endogenous steroid. Nature 392, 926-930.
91. A receptors. Proc Natl Acad Sci U S A 100, 14439-14444.
92. A conductances in hippocampal neurons. J Neurosci 22, RC223.
93. Stemmler M & Koch C (1999). How voltage-dependent conductances can adapt to maximize the information encoded by neuronal firing rate. Nat Neurosci 2, 521-527.
94. A receptors are a target for alcohol. Nat Neurosci 5, 721-722.
95. Tossman U, Jonsson G & Ungerstedt U (1986). Regional distribution and extracellular levels of amino acids in rat central nervous system. Acta Physiol Scand 127, 533-545.
96. Turrigiano GG (1999). Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci 22, 221-227.
97. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC & Nelson SB (1998). Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892-896.
98. Turrigiano GG & Nelson SB (2000). Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol 10, 358-364.
99. A receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur J Neurosci 9, 533-548.
100. A receptors at low concentrations known to have effects in humans. Proc Natl Acad Sci U S A 100, 15218-15223.
101. A receptor function by tyrosine phosphorylation of β subunits. J Neurosci 17, 5062-5069.
102. A receptors to postsynaptic domains by insulin. Nature 388, 686-690.
103. Wang J, Liu S, Haditsch U, Tu W, Cochrane K, Ahmadian G, Tran L, Paw J, Wang Y, Mansuy I, Salter MW & Lu YM (2003a). Interaction of calcineurin and type-A GABA receptor gamma 2 subunits produces long-term depression at CA1 inhibitory synapses. J Neurosci 23 826-836.
104. Wang Q, Liu L, Pei L, Ju W, Ahmadian G, Lu J, Wang Y, Liu F & Wang YT (2003b). Control of synaptic strength, a novel function of Akt. Neuron 38, 915-928.
105. A receptors in hippocampal neurons. J Neurosci 24, 8379-8382.
106. Werhahn KJ, Kunesch E, Noachtar S, Benecke R & Classen J (1999). Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol 517, 591-597.
107. A receptor α6 subunit in hippocampal pyramidal neurons produces extrasynaptic receptors and an increased tonic inhibition. Neuropharmacology 43, 530-549.
108. A receptors containing the delta subunit. J Neurosci 22, 1541-1549.
109. A receptors in hippocampal neurons are high-affinity, low-conductance sensors for extracellular GABA. Mol Pharmacol 63, 2-8.
110. A receptors. J Neurosci 16, 6648-6656.