Postdepolarization potentiation of GABAA receptors: A novel mechanism regulating tonic conductance in hippocampal neurons

Journal of Neuroscience

Volumn 30, Issue 22, 2010, Pages 7672-7684

  Ransom, Christopher B ^a,b   Wu, Yuanming ^a   Richerson, George B ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ANION; 1 (2 (TRIS(4 METHOXYPHENYL)METHOXY)ETHYL) 3 PIPERIDINECARBOXYLIC ACID; 1 (4,4 DIPHENYL 3 BUTENYL)NIPECOTIC ACID; 1-(2-(TRIS(4-METHOXYPHENYL)METHOXY)ETHYL)-3-PIPERIDINECARBOXYLIC ACID; 4 AMINOBUTYRIC ACID CARRIER; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; ANISOLE DERIVATIVE; BICUCULLINE; N-(4,4-DIPHENYL-3-BUTENYL)NIPECOTIC ACID; NIPECOTIC ACID DERIVATIVE;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL CULTURE; CONDUCTANCE; CONTROLLED STUDY; DEPOLARIZATION; ELECTRIC POTENTIAL; EPILEPTIC DISCHARGE; EXCITABILITY; FEMALE; HIPPOCAMPUS; ISCHEMIA; MALE; NONHUMAN; PATCH CLAMP; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT; SEIZURE; SYNAPSE VESICLE; TIME; VOLTAGE CLAMP; ANIMAL; BIOPHYSICS; CELL MEMBRANE POTENTIAL; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ELECTROSTIMULATION; METHODOLOGY; NERVE CELL; NEWBORN; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; ANISOLES; BICUCULLINE; BIOPHYSICAL PROCESSES; BIOPHYSICS; CELLS, CULTURED; ELECTRIC STIMULATION; GABA ANTAGONISTS; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; HIPPOCAMPUS; MEMBRANE POTENTIALS; NEURONS; NIPECOTIC ACIDS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A;

EID: 77953210683     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0290-10.2010     Document Type: Article

References (66)

1. Allen NJ, Rossi DJ, Attwell D (2004) Sequential release of GABA by exocytosis and reversed uptake leads to neuronal swelling in simulated ischemia of hippocampal slices. J Neurosci 24:3837-3849.
2. Ashwood TJ, Collingridge GL, Herron CE, Wheal HV (1987) Voltageclamp analysis of somatic gamma-aminobutyric acid responses in adult rat hippocampal CA1 neurones in vitro. J Physiol 384:27-37.
3. A receptors containing the δ subunit. Neuropharmacology 43:492-502.
4. A receptors regulate the intrinsic excitability of mouse hippocampal pyramidal neurons. J Neurophysiol 98:2244-2254.
5. Bormann J, Hamill OP, Sakmann B (1987) Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones. J Physiol 385:243-286.
6. A receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway. J Biol Chem 275:38856-38862.
7. 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.
8. Burgard EC, Tietz EI, Neelands TR, Macdonald RL (1996) Properties of recombinant gamma-aminobutyric acid A receptor isoforms containing the α5 subunit subtype. Mol Pharmacol 50:119-127.
9. A receptor channels by the 5-HT4 receptor-mediated signalling in rat prefrontal cortical pyramidal neurons. J Physiol 540:743-759.
10. Chabwine JN, Van Damme P, Eggermont J, De Smedt H, Missiaen L, Van Den Bosch L, Parys JB, Robberecht W, Callewaert G (2004) Long-lasting changes in GABA responsiveness in cultured neurons. Neurosci Lett 365:69-72.
11. Chadderton P, Margrie TW, Häusser M (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature 428:856-860.
12. A receptor clustering and modulates the channel kinetics. Proc Natl Acad Sci U S A 97:11557-11562.
13. A receptors mediate the amnestic but not sedative-hypnotic effects of the general anesthetic etomidate. J Neurosci 26:3713-3720.
14. A receptor-mediated tonic inhibition in thalamic neurons. J Neurosci 25:11553-11563.
15. Curmi JP, Premkumar LS, Birnir B, Gage PW (1993) The influence of membrane potential on chloride channels activated by GABA in rat cultured hippocampal neurons. J Membr Biol 136:273-280.
16. A receptors enhances cognition. J Pharmacol Exp Ther 316:1335-1345.
17. Doiron B, Longtin A, Berman N, Maler L (2001) Subtractive and divisive inhibition: effect of voltage-dependent inhibitory conductances and noise. Neural Comput 13:227-248.
18. During MJ, Spencer DD (1993) Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341:1607-1610.
19. A receptor-associated protein. J Biol Chem 279:21701-21706.
20. A receptors. Nat Rev Neurosci 6:215-229.
21. Fatima-Shad K, Barry PH (1993) Anion permeation in GABA- and glycinegated channels of mammalian cultured hippocampal neurons. Proc Biol Sci 253:69-75.
22. A receptor activity by voltage. Mol Cell Neurosci 20:683-694.
23. Fujiwara-Tsukamoto Y, Isomura Y, Imanishi M, Fukai T, Takada M (2007) Distinct types of ionic modulation ofGABAactions in pyramidal cells and interneurons during electrical induction of hippocampal seizure-like network activity. Eur J Neurosci 25:2713-2725.
24. Gaspary HL, Wang W, Richerson GB (1998) Carrier-mediated GABA release activates GABA receptors on hippocampal neurons. J Neurophysiol 80:270-281.
25. A receptor α5 subunit-deficient mice. J Neurophysiol 95:2796-2807.
26. Glykys J, Mody I (2007) The main source of ambient GABA responsible for tonic inhibition in the mouse hippocampus. J Physiol 582:1163-1178.
27. A receptor subunits are necessary for tonic inhibition in the hippocampus? J Neurosci 28:1421-1426.
28. A receptors during status epilepticus. J Neurosci 28:2527-2538.
29. Gray R, Johnston D (1985) Rectification of single GABA-gated chloride channels in adult hippocampal neurons. J Neurophysiol 54:134-142.
30. A-receptor desensitization in cultured chick cerebral neurons. Synapse 12:169-171.
31. Hamann M, Rossi DJ, Attwell D (2002) Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33:625-633.
32. A receptor in the pilocarpine model of temporal lobe epilepsy. Hippocampus 13:633-645.
33. - accumulation responsible for depolarizing GABAergic responses in mature hippocampal neurons. J Neurophysiol 90:2752-2756.
34. Jones MV, Westbrook GL (1997) Shaping of IPSCs by endogenous calcineurin activity. J Neurosci 17:7626-7633.
35. A receptor-associated protein underlies long-term potentiation at inhibitory synapses on a cerebellar Purkinje neuron. J Neurosci 27:6788-6799.
36. A conductances in rat neocortex. J Neurophysiol 94:2073-2085.
37. Kullmann DM, Semyanov A (2002) Glutamatergic modulation of GABAergic signaling among hippocampal interneurons: novel mechanisms regulating hippocampal excitability. Epilepsia 43 [Suppl 5]:S174-S178.
38. A receptors. Soc Neurosci Abstr 29:48.2.
39. A receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat Neurosci 8:797-804.
40. A receptors. J Neurosci 27:14326-14337.
41. Mellor JR, Randall AD (1998) Voltage-dependent deactivation and desensitization of GABA responses in cultured murine cerebellar granule cells. J Physiol 506:377-390.
42. Mitchell SJ, Silver RA (2003) Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38:433-445.
43. Oh DJ, Dichter MA (1992) Desensitization of GABA-induced currents in cultured rat hippocampal neurons. Neuroscience 49:571-576.
44. A receptors in pyramidal cells modulate neuronal offset, not gain. J Neurosci 29:15341-15350.
45. A receptor in a mouse model of temporal lobe epilepsy. J Neurosci 24:8629-8639.
46. A receptor function by PKA and PKC in adult hippocampal neurons. J Neurosci 19:674-683.
47. Pytel M, Mozrzymas JW (2006) Membrane voltage differently affects mIPSCs and current responses recorded from somatic excised patches in rat hippocampal cultures. Neurosci Lett 393:189-193.
48. A receptor gating in cultured rat hippocampal neurons. Neuropharmacology 50:143-153.
49. Radcliffe KA, Fisher JL, Gray R, Dani JA (1999) Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons. Ann N Y Acad Sci 868:591-610.
50. Richerson GB, Wu Y (2003) Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J Neurophysiol 90:1363-1374.
51. Rossi DJ, Hamann M, Attwell D (2003) Multiple modes of GABAergic inhibition of rat cerebellar granule cells. J Physiol 548:97-110.
52. A receptor currents in the hippocampus. J Neurosci 25:10016-10024.
53. - ion conductance. J Neurophysiol 51:500-515.
54. Semyanov A, Walker MC, Kullmann DM (2003) GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6:484-490.
55. A receptors: modulating gain and maintaining the tone. Trends Neurosci 27:262-269.
56. A receptors triggers anxiety at puberty. Nat Neurosci 10:469-477.
57. Sjöström PJ, Rancz EA, Roth A, Häusser M (2008) Dendritic excitability and synaptic plasticity. Physiol Rev 88:769-840.
58. A receptors. Science 269:977-981.
59. Wanaverbecq N, Semyanov A, Pavlov I, Walker MC, Kullmann DM (2007) Cholinergic axons modulate GABAergic signaling among hippocampal interneurons via postsynaptic α7 nicotinic receptors. J Neurosci 27:5683-5693.
60. Weiss DS (1988) Membrane potential modulates the activation of GABA-gated channels. J Neurophysiol 59:514-527.
61. Wu Y, Wang W, Richerson GB (2001) GABA transaminase inhibition induces spontaneous and enhances depolarization-evoked GABA efflux via reversal of the GABA transporter. J Neurosci 21:2630-2639.
62. Wu Y, Wang W, Richerson GB (2003) Vigabatrin induces tonic inhibition via GABA transporter reversal without increasing vesicular GABA release. J Neurophysiol 89:2021-2034.
63. Wu Y, Wang W, Richerson GB (2006) The transmembrane sodium gradient influences ambient GABA concentration by altering the equilibrium of GABA transporters. J Neurophysiol 96:2425-2436.
64. Wu Y, Wang W, Díez-Sampedro A, Richerson GB (2007) Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56:851-865.
65. A receptor channel desensitization in rat hippocampal neurons. J Neurophysiol 71:2151-2160.
66. A receptor subunits on dentate granule cell dendrites influences tonic and phasic inhibition in a mouse model of epilepsy. J Neurosci 27:7520-7531.