Single and repetitive paired-pulse suppression: A parametric analysis and assessment of usefulness in epilepsy research

Epilepsia

Volumn 50, Issue 4, 2009, Pages 904-916

  Waldbaum, Simon ^a,b   Dudek, F Edward ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Dentate gyrus; GABA; Hippocampus; Inhibition

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL PROTOCOL; DENTATE GYRUS; EPILEPSY; GABAERGIC TRANSMISSION; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; NERVE STIMULATION; NEUROLOGICAL AND SENSORIAL PROCEDURES; NONHUMAN; PAIRED PULSE TECHNIQUE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; SPIKE WAVE;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BIOPHYSICAL PHENOMENA; BIOPHYSICS; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; EPILEPSY; MALE; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 63849109992     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2008.01939.x     Document Type: Article

References (62)

1. Alger BE, Teyler TJ 1976) Long-term and short-term plasticity in the CA1, CA3, and dentate regions of the rat hippocampal slice. Brain Res 110 : 463 480.
2. Andersen P, Lomo T 1967) Control of hippocampal output by afferent volley frequency. Prog Brain Res 27 : 400 412.
3. Andersen P, Eccles JC, Loyning Y 1964) Location of postsynaptic inhibitory synapses on hippocampal pyramids. J Neurophysiol 27 : 592 607.
4. Andersen P, Holmqvist B, Voorhoeve PE 1966) Entorhinal activation of dentate granule cells. Acta Physiol Scand 66 : 448 460.
5. Babb TL, Pretorius JK, Kupfer WR, Crandall PH 1989) Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. J Neurosci 9 : 2562 2574.
6. Bausch SB 2005) Axonal sprouting of GABAergic interneuron in temporal lobe epilepsy. Epilepsy Behav 7 : 390 400.
7. Ben-Ari Y, Krnjevic K, Reinhardt W 1979) Hippocampal seizures and failure of inhibition. Can J Physiol Pharmacol 57 : 1462 1466.
8. Bragin A, Azizyan A, Almajano J, Wilson CL, Engel J 2005) Analysis of chronic seizure onsets after intrahippocampal kainic acid injection in freely moving rats. Epilepsia 46 : 1592 1598.
9. Brooks-Kayal AR, Shumate MD, Jin H, Rikhter TY, Coulter DA 1998) Selective changes in single cell GABA (A) receptor subunit expression and function in temporal lobe epilepsy. Nat Med 4 : 1166 1172.
10. Buckmaster PS, Dudek FE 1997) Network properties of the dentate gyrus in epileptic rats with hilar neuron loss and granule cell axon reorganization. J Neurophysiol 5 : 2685 2696.
11. 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.
12. Davenport CJ, Brown WJ, Babb TL 1990) GABAergic neurons are spared after intrahippocampal kainate in the rat. Epilepsy Res 5 : 28 42.
13. Franck JE, Pokorny J, Kunkel DD, Schwartzkroin PA 1995) Physiologic and morphologic characteristics of granule cell circuitry in human epileptic hippocampus. Epilepsia 36 : 543 558.
14. Gibbs JW, Sombati S, DeLorenzo RJ, Coulter DA 1997a) Physiological and pharmacological alterations in postsynaptic GABA(A) receptor function in a hippocampal culture of chronic spontaneous seizures. J Neurophysiol 77 : 2139 2152.
15. Gibbs JW, Shumate MD, Coulter DA 1997b) Differential epilepsy-associated alterations in postsynaptic GABA(A) receptor function in dentate granule and CA1 neurons. J Neurophysiol 77 : 1924 2138.
16. Haas KZ, Sperber EF, Moshe SL, Stanton PK 1996) Kainic acid-induced seizures enhance dentate gyrus inhibition by downregulation of GABA(B) receptors. J Neurosci 16 : 4250 4260.
17. Harvey BD, Sloviter RS 2005) Hippocampal granule cell activity and c-Fos expression during spontaneous seizures in awake, chronically epileptic, pilocarpine-treated rats: implications for hippocampal epileptogenesis. J Comp Neurol 488 : 442 463.
18. Hellier J., Patrylo PR, Dou P, Nett M, Rose GM, Dudek FE 1999) Assessment of inhibition and epileptiform activity in the septal dentate gyrus of freely behaving rats during the first week after kainate treatment. J Neurosci 19 : 10053 10064.
19. Isokawa-Akesson M, Wilson CL, Babb TL 1989) Inhibition in synchronously firing human hippocampal neurons. Epilepsy Res 3 : 236 247.
20. de Jonge M, Racine RJ 1987) The development and decay of kindling-induced increases in paired-pulse depression in the dentate gyrus. Brain Res 412 : 318 328.
21. Joy RM, Albertson TE 1987) Interactions of lindane with synaptically mediated inhibition and facilitation in the dentate gyrus. Neurotoxicology 8 : 529 542.
22. Kamphuis W, Gorter JA, Wadman WJ, Lopes da Silva FH 1992) Hippocampal kindling leads to different changes in paired-pulse depression of local evoked field potentials in CA1 area and in fascia dentata. Neurosci Lett 141 : 101 105.
23. A receptors. J Neurosci 17 : 7532 7540.
24. Kapur J, Stringer JL, Lothman EW 1989) Evidence that repetitive seizures in the hippocampus cause a lasting reduction of GABAergic inhibition. J Neurophysiol 61 : 417 426.
25. King GL, Dingledine R, Giacchino JL, McNamara J 1985) Abnormal neuronal excitability in hippocampal slices from kindled rats. J Neurophysiol 54 : 1295 1304.
26. Kotti T, Riekkinen PJ, Miettinen R 1997) Characterization of target cells for aberrant mossy fiber collaterals in the dentate gyrus of epileptic rat. Exp Neurol 146 : 323 330.
27. + activity accompanying hippocampal discharges. Can J Physiol Pharmacol 58 : 579 583.
28. Lee HK, Dunwiddie T, Hoffer B 1980) Electrophysiological interactions of enkephalins with neuronal circuitry in the rat hippocampus. II. Effects on interneuron excitability. Brain Res 184 : 331 342.
29. Maru E, Goddard GV 1987) Alteration in dentate neuronal activities associated with perforant path kindling III: enhancement of synaptic inhibition. Exp Neurol 96 : 46 60.
30. Matthews WD, McCafferty GP, Setler PE 1981) An electrophysiological model of GABA-mediated neurotransmission. Neuropharmacol 20 : 561 565.
31. McCarren M, Alger BA 1985) Use-dependent depression of IPSPs in rat hippocampal pyramidal cells in vitro. J Neurophysiol 53 : 557 571.
32. McCormick DA 1989) GABA as an inhibitory neurotransmitter in human cerebral cortex. J Neurophysiol 62 : 1018 1027.
33. Miles R, Wong RK 1987) Latent synaptic pathways revealed after tetanic stimulation in the hippocampus. Nature 329 : 724 726.
34. Milgram NW, Yearwood T, Khurgel M, Ivy GO, Racine R 1991) Changes in inhibitory processes in the hippocampus following recurrent seizures induced by systemic administration of kainic acid. Brain Res 551 : 236 246.
35. Mohler H, Fritschy JM, Luscher B, Rudolph U, Benson J, Benke D 1996) The GABAA receptors. From subunits to diverse functions. Ion Channels 4 : 89 113.
36. A receptors underlies potentiation at hippocampal inhibitory synapses. Nature 395 : 172 177.
37. Oliver MW, Miller JJ 1985) Alterations of inhibitory processes in the dentate gyrus following kindling-induced epilepsy. Exp Brain Res 57 : 443 447.
38. Otis TS, DeKoninck Y, Mody I 1994) Lasting potentiation of inhibition is associated with an increased number of GABA type A receptors activated during miniature inhibitory postsynaptic currents. Proc Natl Acad Sci U S A 91 : 7698 7702.
39. Prince DA 1968) Inhibition in focal epileptogenesis. Electroencephalogr Clin Neurophysiol 24 : 290.
40. Racine RJ, Milgram NW 1983) Short-term potentiation phenomena in the rat limbic forebrain. Brain Res 260 : 201 216.
41. Ribak CE, Peterson GM 1991) Intragranular mossy fibers in rats and gerbils form synapses with the somata and proximal dendrites of basket cells in the dentate gyrus. Hippocampus 1 : 355 364.
42. Ribak CE, Harris B, Vaughn JE, Roberts E 1979) Inhibitory, GABAergic nerve terminals decrease at sites of focal epilepsy. Science 205 : 211 214.
43. Sayin U, Rutecki PA, Mellanby J, Sutula TP 2001) Gamma-vinyl GABA reduces paired pulse inhibition in the rat dentate gyrus in vivo and in vitro. Epilepsy Res 44 : 109 117.
44. Shao LR, Dudek FE 2005) Changes in mIPSC's and sIPCS's after kainite treatment: evidence for loss of inhibitory input to dentate granule cells and possible compensatory responses. J Neurophysiol 94 : 952 960.
45. Sloviter RS 1983) "Epileptic" brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res Bull 10 : 675 697.
46. Sloviter RS 1991a) Feedforward and feedback inhibition of hippocampal principal cell activity evoked by perforant path stimulation: GABA-mediated mechanisms that regulate excitability in vivo. Hippocampus 1 : 31 40.
47. Sloviter RS 1991b) Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the "dormant basket cell" hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1 : 41 66.
48. Sloviter RS 1992) Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci Lett 137 : 91 96.
49. Sloviter RS, Damiano BP 1981a) Sustained electrical stimulation of the perforant path duplicates kainate-induced electrophysiological effects and hippocampal damage in rats. Neurosci Lett 24 : 279 284.
50. Sloviter RS, Damiano BP 1981b) On the relationship between kainic acid-induced epileptiform activity and hippocampal neuronal damage. Neuropharmacology 20 : 1003 1011.
51. Sloviter RS, Zappone CA, Harvey BD, Frotscher M 2006) Kainic acid-induced recurrent mossy fiber innervation of dentate gyrus inhibitory interneurons: possible anatomical substrate of granule cell hyper-inhibition in chronically epileptic rats. J Comp Neurol 494 : 944 960.
52. Staley KJ, Mody I 1992) Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor-mediated postsynaptic conductance. J Neurophysiol 68 : 197 212.
53. Stringer JL, Lothman EW 1989) Repetitive seizures cause an increase in paired-pulse inhibition in the dentate gyrus. Neurosci Lett 105 : 91 95.
54. Swanson TH, Sperling MR, O'Connor MJ 1998) Strong paired pulse depression of dentate granule cells in slices from patients with temporal lobe epilepsy. J Neural Transm 105 : 613 625.
55. Tauck DL, Nadler JV 1985) Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid treated rats. J Neurosci 5 : 1016 1022.
56. Thalmann RH, Ayala GF 1982) A late increase in potassium conductance follows synaptic stimulation of granule neurons of the dentate gyrus. Neurosci Lett 29 : 243 248.
57. Thompson SM, Gahwiler BH 1989) Activity-dependent disinhibition. I. Repetitive stimulation reduces IPSP driving force and conductance in the hippocampus in vitro. J Neurophysiol 61 : 501 511.
58. Titulaer MN, Ghijsen WE, Kamphius W, De Rijk TC, Lopes da Silva FH 1995) Opposite changes in GABAA receptor function in the CA1-3 area and fascia dentata of kindled rat hippocampus. J Neurochem 64 : 2615 2621.
59. Tuff LP, Racine RJ, Adamec R 1983) The effects of kindling on GABA-mediated inhibition in the dentate gyrus of the rat. I. Paired-pulse depression. Brain Res 277 : 79 97.
60. Uruno K, O'Connor MJ, Masukawa LM 1994) Alterations of inhibitory synaptic responses in the dentate gyrus of temporal lobe epileptic patients. Hippocampus 4 : 583 593.
61. Wilson CL, Khan SU, Engel J, Isokawa M, Babb TL, Behnke EJ 1998) Paired pulse suppression and facilitation in human epileptogenic hippocampal formation. Epilepsy Res 31 : 211 230.
62. Wuarin JP, Dudek FE 1996) Electropraphic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainite treated epileptic rats. J Neurosci 16 : 4438 4448.