Status epilepticus enhances tonic GABA currents and depolarizes GABA reversal potential in dentate fast-spiking basket cells

Journal of Neurophysiology

Volumn 109, Issue 7, 2013, Pages 1746-1763

  Yu, Jiandong ^a   Proddutur, Archana ^a   Elgammal, Fatima S ^a   Ito, Takahiro ^a   Santhakumar, Vijayalakshmi ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Epilepsy; Interneuron; Tonic inhibition

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR DELTA; 4,5,6,7 TETRAHYDROISOXAZOLO[4,5 C]PYRIDIN 3 OL; PARVALBUMIN; PILOCARPINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASKET CELL; CONTROLLED STUDY; DEPOLARIZATION; EPILEPTIC STATE; HOMEOSTASIS; IMMUNOREACTIVITY; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MALE; MEMBRANE STEADY POTENTIAL; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT;

ACTION POTENTIALS; ANIMALS; DENTATE GYRUS; GABA AGONISTS; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; HOMEOSTASIS; INTERNEURONS; MALE; MEMBRANE POTENTIALS; PILOCARPINE; RATS; RATS, WISTAR; RECEPTORS, GABA-A; STATUS EPILEPTICUS;

EID: 84878499405     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00891.2012     Document Type: Article

References (77)

1. Arima-Yoshida F, Watabe AM, Manabe T. The mechanisms of the strong inhibitory modulation of long-term potentiation in the rat dentate gyrus. Eur J Neurosci 33: 1637-1646, 2011.
2. Baldi R, Varga C, Tamas G. Differential distribution of KCC2 along the axo-somato-dendritic axis of hippocampal principal cells. Eur J Neurosci 32: 1319-1325, 2010.
3. Banke TG, McBain CJ. GABAergic input onto CA3 hippocampal interneurons remains shunting throughout development. J Neurosci 26: 11720-11725, 2006.
4. Bartos M, Vida I, Frotscher M, Geiger JR, Jonas P. Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J Neurosci 21: 2687-2698, 2001.
5. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JR, Jonas P. Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Natl Acad Sci USA 99: 13222-13227, 2002.
6. Ben-Ari Y. Developing networks play a similar melody. Trends Neurosci 24: 353-360, 2001.
7. Bianchi MT, Macdonald RL. Agonist trapping by GABAA receptor channels. J Neurosci 21: 9083-9091, 2001.
8. Billups D, Attwell D. Control of intracellular chloride concentration and GABA response polarity in rat retinal ON bipolar cells. J Physiol 545: 183-198, 2002.
9. Bragin A, Wilson CL, Almajano J, Mody I, Engel J Jr. High-frequency oscillations after status epilepticus: epileptogenesis and seizure genesis. Epilepsia 45: 1017-1023, 2004.
10. 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.
11. A receptor subunit expression and function in temporal lobe epilepsy. Nat Med 4: 1166-1172, 1998.
12. A receptors. Br J Pharmacol 136: 965-974, 2002.
13. Buckmaster PS, Yamawaki R, Zhang GF. Axon arbors and synaptic connections of a vulnerable population of interneurons in the dentate gyrus in vivo. J Comp Neurol 445: 360-373, 2002.
14. Buzsaki G. Rhythms of the Brain. New York: Oxford Univ. Press, 2006.
15. Cossart R, Bernard C, Ben-Ari Y. Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies. Trends Neurosci 28: 108-115, 2005.
16. Coulter DA. Epilepsy-associated plasticity in gamma-aminobutyric acid receptor expression, function, and inhibitory synaptic properties. Int Rev Neurobiol 45: 237-252, 2001.
17. Coulter DA, Carlson GC. Functional regulation of the dentate gyrus by GABA-mediated inhibition. Prog Brain Res 163: 235-243, 2007.
18. Duguid I, Branco T, London M, Chadderton P, Hausser M. Tonic inhibition enhances fidelity of sensory information transmission in the cerebellar cortex. J Neurosci 32: 11132-11143, 2012.
19. Dyhrfjeld-Johnsen J, Santhakumar V, Morgan RJ, Huerta R, Tsimring L, Soltesz I. Topological determinants of epileptogenesis in large-scale structural and functional models of the dentate gyrus derived from experimental data. J Neurophysiol 97: 1566-1587, 2007.
20. Dzhala V, Valeeva G, Glykys J, Khazipov R, Staley K. Traumatic alterations in GABA signaling disrupt hippocampal network activity in the developing brain. J Neurosci 32: 4017-4031, 2012.
21. Ebihara S, Shirato K, Harata N, Akaike N. Gramicidin-perforated patch recording: GABA response in mammalian neurones with intact intracellular chloride. J Physiol 484: 77-86, 1995.
22. Ekstrand JJ, Pouliot W, Scheerlinck P, Dudek FE. Lithium pilocarpineinduced status epilepticus in postnatal day 20 rats results in greater neuronal injury in ventral versus dorsal hippocampus. Neuroscience 192: 699-707, 2011.
23. Ewell LA, Jones MV. Frequency-tuned distribution of inhibition in the dentate gyrus. J Neurosci 30: 12597-12607, 2010.
24. Farrant M, Nusser Z. Variations on an inhibitory theme: phasic and tonic activation of GABAA receptors. Nat Rev Neurosci 6: 215-229, 2005.
25. Freund TF. Interneuron Diversity series: Rhythm and mood in perisomatic inhibition. Trends Neurosci 26: 489-495, 2003.
26. Fricker D, Verheugen JA, Miles R. Cell-attached measurements of the firing threshold of rat hippocampal neurones. J Physiol 517: 791-804, 1999.
27. A-ergic neurons and GABAA-receptors in temporal lobe epilepsy. Neurochem Int 34: 435-445, 1999.
28. Geiger JR, Lubke J, Roth A, Frotscher M, Jonas P. Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18: 1009-1023, 1997.
29. Glykys J, Mody I. The main source of ambient GABA responsible for tonic inhibition in the mouse hippocampus. J Physiol 582: 1163-1178, 2007.
30. Glykys J, Peng Z, Chandra D, Homanics GE, Houser CR, Mody I. A new naturally occurring GABAA receptor subunit partnership with high sensitivity to ethanol. Nat Neurosci 10: 40-48, 2007.
31. Gupta A, Elgammal FS, Proddutur A, Shah S, Santhakumar V. Decrease in tonic inhibition contributes to increase in dentate semilunar granule cell. J Neurosci 32: 2523-2537, 2012.
32. Harney SC, Jones MV. Preand postsynaptic properties of somatic and dendritic inhibition in dentate gyrus. Neuropharmacology 43: 584-594, 2002.
33. Hefft S, Jonas P. Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8: 1319-1328, 2005.
34. Hines ML, Carnevale NT. The NEURON simulation environment. Neural Comput 9: 1179-1209, 1997.
35. Howard AL, Neu A, Morgan RJ, Echegoyen JC, Soltesz I. Opposing modifications in intrinsic currents and synaptic inputs in post-traumatic mossy cells: evidence for single-cell homeostasis in a hyperexcitable network. J Neurophysiol 97: 2394-2409, 2007.
36. Kobayashi M, Buckmaster PS. Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J Neurosci 23: 2440-2452, 2003.
37. Kobayashi M, Wen X, Buckmaster PS. Reduced inhibition and increased output of layer II neurons in the medial entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 23: 8471-8479, 2003.
38. Kraushaar U, Jonas P. Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse. J Neurosci 20: 5594-5607, 2000.
39. Krook-Magnuson EI, Li P, Paluszkiewicz SM, Huntsman MM. Tonically active inhibition selectively controls feedforward circuits in mouse barrel cortex. J Neurophysiol 100: 932-944, 2008.
40. Mann EO, Mody I. Control of hippocampal gamma oscillation frequency by tonic inhibition and excitation of interneurons. Nat Neurosci 13: 205-212, 2010.
41. Marder E. Variability, compensation, and modulation in neurons and circuits. Proc Natl Acad Sci USA 108, Suppl 3: 15542-15548, 2011.
42. Margerison JH, Corsellis JA. Epilepsy and the temporal lobes. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 89: 499-530, 1966.
43. McBain CJ, Eaton JV, Brown T, Dingledine R. CNQX increases spontaneous inhibitory input to CA3 pyramidal neurones in neonatal rat hippocampal slices. Brain Res 592: 255-260, 1992.
44. Meldrum BS, Rogawski MA. Molecular targets for antiepileptic drug development. Neurotherapeutics 4: 18-61, 2007.
45. Mello LE, Cavalheiro EA, Tan AM, Kupfer WR, Pretorius JK, Babb TL, Finch DM. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34: 985-995, 1993.
46. Mitchell SJ, Silver RA. Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38: 433-445, 2003.
47. Morgan RJ, Soltesz I. Nonrandom connectivity of the epileptic dentate gyrus predicts a major role for neuronal hubs in seizures. Proc Natl Acad Sci USA 105: 6179-6184, 2008.
48. Mtchedlishvili Z, Kapur J. High-affinity, slowly desensitizing GABAA receptors mediate tonic inhibition in hippocampal dentate granule cells. Mol Pharmacol 69: 564-575, 2006.
49. Olah S, Fule M, Komlosi G, Varga C, Baldi R, Barzo P, Tamas G. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461: 1278-1281, 2009.
50. Pathak HR, Weissinger F, Terunuma M, Carlson GC, Hsu FC, Moss SJ, Coulter DA. Disrupted dentate granule cell chloride regulation enhances synaptic excitability during development of temporal lobe epilepsy. J Neurosci 27: 14012-14022, 2007.
51. Peng Z, Huang CS, Stell BM, Mody I, Houser CR. Altered expression of the delta subunit of the GABAA receptor in a mouse model of temporal lobe epilepsy. J Neurosci 24: 8629-8639, 2004.
52. Rajasekaran K, Joshi S, Sun C, Mtchedlishvilli Z, Kapur J. Receptors with low affinity for neurosteroids and GABA contribute to tonic inhibition of granule cells in epileptic animals. Neurobiol Dis 40: 490-501, 2010.
53. Raol YS, Budreck EC, Brooks-Kayal AR. Epilepsy after early-life seizures can be independent of hippocampal injury. Ann Neurol 53: 503-511, 2003.
54. - cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol 562: 27-36, 2005.
55. Romo-Parra H, Trevino M, Heinemann U, Gutierrez R. GABA actions in hippocampal area CA3 during postnatal development: differential shift from depolarizing to hyperpolarizing in somatic and dendritic compartments. J Neurophysiol 99: 1523-1534, 2008.
56. Rossi DJ, Hamann M, Attwell D. Multiple modes of GABAergic inhibition of rat cerebellar granule cells. J Physiol 548: 97-110, 2003.
57. Santhakumar V. Modeling mossy cell loss and mossy fiber sprouting in epilepsy. In: Computational Neuroscience in Epilepsy, edited by Soltesz I, Staley KJ. San Diego, CA: Academic, 2008, p. 89-111.
58. Santhakumar V, Aradi I, Soltesz I. Role of mossy fiber sprouting and mossy cell loss in hyperexcitability: a network model of the dentate gyrus incorporating cell types and axonal topography. J Neurophysiol 93: 437-453, 2005.
59. Santhakumar V, Bender R, Frotscher M, Ross ST, Hollrigel GS, Toth Z, Soltesz I. Granule cell hyperexcitability in the early post-traumatic rat dentate gyrus: the "irritable mossy cell" hypothesis. J Physiol 524: 117-134, 2000.
60. Santhakumar V, Hanchar HJ, Wallner M, Olsen RW, Otis TS. Contributions of the GABAA receptor alpha6 subunit to phasic and tonic inhibition revealed by a naturally occurring polymorphism in the alpha6 gene. J Neurosci 26: 3357-3364, 2006.
61. Santhakumar V, Jones RT, Mody I. Developmental regulation and neuroprotective effects of striatal tonic GABAA currents. Neuroscience 167: 644-655, 2010.
62. Santhakumar V, Ratzliff AD, Jeng J, Toth K, Soltesz I. Long-term hyperexcitability in the hippocampus after experimental head trauma. Ann Neurol 50: 708-717, 2001.
63. Sauer JF, Bartos M. Recruitment of early postnatal parvalbumin-positive hippocampal interneurons by GABAergic excitation. J Neurosci 30: 110-115, 2010.
64. Scimemi A, Semyanov A, Sperk G, Kullmann DM, Walker MC. Multiple and plastic receptors mediate tonic GABAA receptor currents in the hippocampus. J Neurosci 25: 10016-10024, 2005.
65. Semyanov A, Walker MC, Kullmann DM. GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6: 484-490, 2003.
66. A conductance in hippocampal interneurons. Nat Commun 2: 376, 2011.
67. Areceptors. Proc Natl Acad Sci USA 100: 14439-14444, 2003.
68. Turrigiano G, Abbott LF, Marder E. Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264: 974-977, 1994.
69. Verheugen JA, Fricker D, Miles R. Noninvasive measurements of the membrane potential and GABAergic action in hippocampal interneurons. J Neurosci 19: 2546-2555, 1999.
70. Vida I, Bartos M, Jonas P. Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49: 107-117, 2006.
71. A receptors and their activation by GABA spillover in the mouse dentate gyrus. J Neurosci 23: 10650-10661, 2003.
72. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482-497, 1991.
73. Zhan RZ, Nadler JV. Enhanced tonic GABA current in normotopic and hilar ectopic dentate granule cells after pilocarpine-induced status epilepticus. J Neurophysiol 102: 670-681, 2009.
74. Zhang N, Wei W, Mody I, Houser CR. Altered localization of GABAA receptor subunits on dentate granule cell dendrites influences tonic and phasic inhibition in a mouse model of epilepsy. J Neurosci 27: 7520-7531, 2007.
75. Zhang W, Buckmaster PS. Dysfunction of the dentate basket cell circuit in a rat model of temporal lobe epilepsy. J Neurosci 29: 7846-7856, 2009.
76. Zhang W, Huguenard JR, Buckmaster PS. Increased excitatory synaptic input to granule cells from hilar and CA3 regions in a rat model of temporal lobe epilepsy. J Neurosci 32: 1183-1196, 2012.
77. Zhang W, Yamawaki R, Wen X, Uhl J, Diaz J, Prince DA, Buckmaster PS. Surviving hilar somatostatin interneurons enlarge, sprout axons, and form new synapses with granule cells in a mouse model of temporal lobe epilepsy. J Neurosci 29: 14247-14256, 2009.