Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy

Journal of Neuroscience

Volumn 23, Issue 6, 2003, Pages 2440-2452

  Kobayashi, Masayuki ^a,b   Buckmaster, Paul S ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Basal dendrites; Dentate gyrus; GABA; GAD; Hippocampus; Interneurons; IPSCs; IPSPs; Mossy fiber sprouting; Paired pulse; Parvalbumin; Somatostatin

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; GENE PRODUCT; GLUTAMATE DECARBOXYLASE 65; MESSENGER RNA; PARVALBUMIN; PILOCARPINE; SOMATOSTATIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; EPILEPTIC DISCHARGE; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC SYSTEM; GRANULE CELL; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MALE; MONOSYNAPTIC POTENTIAL; NERVE CELL INHIBITION; NERVE CONDUCTION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; RAT; RECURRENT DISEASE; SEIZURE; SYNAPTIC INHIBITION; SYNAPTOGENESIS; TEMPORAL LOBE EPILEPSY;

EID: 0037444634     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-06-02440.2003     Document Type: Article

References (81)

1. Andre V, Marescaux C, Nehlig A, Fritschy JM (2001) Alterations of hippocampal GABAergic system contribute to spontaneous recurrent seizures in the rat lithium pilocarpine model of temporal lobe epilepsy. Hippocampus 11:452-468.
2. Babb TL, Brown WJ, Pretorius J, Davenport C, Lieb JP, Crandall PH (1984) Temporal lobe volumetric cell densities in temporal lobe epilepsy. Epilepsia 25:729-740.
3. Babb TL, Pretorius JK, Kupfer WR, Crandall PH (1989) Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. J Neurosci 9:2562-2574.
4. A,slow J Neurosci 18:1305-1317.
5. Bragin A, Engel Jr JE, Wilson CL, Fried I, Mathern GW (1999) Hippocampal and entorhinal cortex high-frequency oscillations (100-500 Hz) in human epileptic brain and in kainic acid-treated rats with chronic seizures. Epilepsia 40:127-137.
6. Buckmaster PS, Dudek FE (1997) Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J Comp Neurol 385:385-404.
7. Buckmaster PS, Dudek FE (1999) In vivo intracellular analysis of granule cell axon reorganization in epileptic rats. J Neurophysiol 81:712-721.
8. Buckmaster PS, Jongen-Rêlo (1999) Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J Neurosci 19:9519-9529.
9. Buckmaster PS, Yamawaki R, Zhang GF (2002a) Axon arbors and synaptic connections of a vulnerable population of interneurons in the dentate gyrus in vivo. J Comp Neurol 445:360-373.
10. Buckmaster PS, Zhang GF, Yamawaki R (2002b) Axon sprouting in a model of temporal lobe epilepsy creates a predominantly excitatory feedback circuit. J Neurosci 22:6650-6658.
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. Cavazos JE, Golarai G, Sutula TP (1992) Septotemporal variation of the supragranular projection of the mossy fiber pathway in the dentate gyrus of normal and kindled rats. Hippocampus 2:363-372.
13. Chagnac-Amitai Y, Connors BW (1989a) Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J Neurophysiol 61:747-758.
14. Chagnac-Amitai Y, Connors BW (1989b) Synchronized excitation and inhibition driven by intrinsically bursting neurons in neocortex. J Neurophysiol 61:149-1162.
15. Colder BW, Wilson CL, Frysinger RC, Chao LC, Harper RM, Engel J Jr (1996) Neuronal synchrony in relation to burst discharge in epileptic human temporal lobes. J Neurophysiol 75:2496-2508.
16. Cossart R, Dinocourt C, Hirsch JC, Merchan-Perez A, De Felipe J, Ben-Ari Y, Esclapez M, Bernard C (2001) Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat Neurosci 4:52-62.
17. Cronin J, Obenaus A, Houser CR, Dudek FE (1992) Electrophysiology of dentate granule cells after kainate-induced synaptic reorganization of the mossy fibers. Brain Res 573:305-310.
18. Davenport CJ, Brown WJ, Babb TL (1990) Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat. Exp Neurol 109:180-190.
19. de Lanerolle NC, Kim JH, Robbins RJ, Spencer DD (1989) Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 495:387-395.
20. Doherty J, Dingledine R (2001) Reduced excitatory drive onto interneurons in the dentate gyrus after status epilepticus. J Neurosci 21:2048-2057.
21. Engel Jr J, Williamson PD, Wieser HG (1997) Mesial temporal lobe epilepsy. In: Epilepsy: a comprehensive textbook. (Engel Jr J, Pedley TA, eds) pp 2417-2426. Philadelphia: Lippincott-Raven.
22. Erlander MG, Tillakaratne NJK, Feldblum S, Patel N, Tobin AJ (1991) Two genes encode distinct glutamate decarboxylases. Neuron 7:91-100.
23. Esclapez M, Houser CR (1999) Up-regulation of GAD65 and GAD67 in remaining hippocampal GABA neurons in a model of temporal lobe epilepsy. J Comp Neurol 412:488-505.
24. Esclapez M, Hirsch JC, Ben-Ari Y, Bernard C (1999) Newly formed excitatory pathways provide a substrate for hyperexcitability in experimental temporal lobe epilepsy. J Comp Neurol 408:449-460.
25. Feldblum S, Ackermann RF, Tobin AJ (1990) Long-term increase of glutamate decarboxylase mRNA in a rat model of temporal lobe epilepsy. Neuron 5:361-371.
26. 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.
27. A receptor function in dentate granule and CA1 neurons. J Neurophysiol 77:1924-1938.
28. Gorter JA, van Vliet EA, Aronica E, Lopes da Silva FH (2001) Progression of spontaneous seizures after status epilepticus is associated with mossy fibre sprouting and extensive bilateral loss of hilar parvalbumin and somatostatin-immunoreactive neurons. Eur J Neurosci 13:657-669.
29. B receptors. J Neurosci 16:4250-4260.
30. Halasy K, Somogyi P (1993) Distribution of GABAergic synapses and their targets in the dentate gyrus of rat: a quantitative immunoelectron microscopic analysis. J Hirnforsch 34:299-308.
31. Hirsch JC, Agassandian C, Merchán-Pérez A, Ben-Ari Y, DeFelipe J, Esclapez M, Bernard C (1999) Deficit of quantal release of GABA in experimental models of temporal lobe epilepsy. Nat Neurosci 2:499-500.
32. Houser CR, Esclapez M (1996) Vulnerability and plasticity of the GABA system in the pilocarpine model of spontaneous recurrent seizures. Epilepsy Res 26:207-218.
33. A receptor-mediated inhibitory postsynaptic currents in dentate granule cells in epileptic hippocampus. J Neurophysiol 75:1901-1908.
34. Isokawa M, Levesque MF (1991) Increased NMDA responses and dendritic degeneration in human epileptic hippocampal neurons in slices. Neurosci Lett 132:212-216.
35. Isokawa-Akesson M, Wilson CE, Babb TL (1989) Inhibition in synchronously firing human hippocampal neurons. Epilepsy Res 3:236-247.
36. Katona I, Acsády L, Freund TF (1999) Postsynaptic targets of somatostatin-immunoreactive interneurons in the rat hippocampus. Neuroscience 88:37-55.
37. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419:119-130.
38. Kraushaar U, Jonas P (2000) Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse. J Neurosci 20:5594-5607.
39. Leranth C, Malcolm AJ, Frotscher M (1990) Afferent and efferent synaptic connections of somatostatin-immunoreactive neurons in the rat fascia dentata. J Comp Neurol 295:111-122.
40. Li H, Prince DA (2002) Synaptic activity in chronically injured, epileptogenic sensory-motor neocortex. J Neurophysiol 88:2-12.
41. Lynch M, Sutula T (2000) Recurrent excitatory connectivity in the dentate gyrus of kindled and kainic acid-treated rats. J Neurophysiol 83:693-704.
42. Margerison JH, Corsellis JAN (1966) 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.
43. Masukawa LM, Wang H, O'Connor MJ, Uruno K (1996) Prolonged field potentials evoked by 1 Hz stimulation in the dentate gyrus of temporal lobe epileptic human brain slices. Brain Res 721:132-139.
44. Mathern GW, Babb TL, Pretorius IK, Leite JP (1995a) Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J Neurosci 15:3990-4004.
45. Mathern GW, Babb TL, Vickrey BG, Melendez M, Pretorius JK (1995b) The clinical-pathogenic mechanisms of hippocampal neuron loss and surgical outcomes in temporal lobe epilepsy. Brain 118:105-118.
46. A receptors. Neuroscience 77:1003-1019.
47. Mathern GW, Pretorius JK, Mendoza D, Lozada A, Kornblum HI (1998) Hippocampal AMPA and NMDA mRNA levels correlate with aberrant fascia dentata mossy fiber sprouting in the pilocarpine model of spontaneous limbic epilepsy. J Neurosci Res 54:734-753.
48. Mello LEA, Cavalheiro EA, Tan AM, Kupfer WR, Pretorius JK, Babb TL, Finch DM (1993) Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34:985-995.
49. Miles R, Wong RKS (1987) Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J Physiol (Lond) 388:611-629.
50. Mody I, Heinemann U (1987) NMDA receptors of dentate gyrus granule cells participate in synaptic transmission following kindling. Nature 326:701-704.
51. Molnár P, Nadler JV (1999) Mossy fiber-granule cell synapses in the normal and epileptic rat dentate gyrus studied with minimal laser photostimulation. J Neurophysiol 82:1883-1894.
52. Molnár P, Nadler JV (2000) γ-Aminobutyrate, α-carboxy-2-nitrobenzyl ester selectively blocks inhibitory synaptic transmission in rat dentate gyrus. Eur J Pharmacol 391:255-262.
53. A receptors in the pilocarpine model of epilepsy. J Neurophysiol 85:1932-1940.
54. Morin F, Beaulieu C, Lacaille J-C (1998) Cell-specific alterations in synaptic properties of hippocampal CA1 interneurons after kainate treatment. J Neurophysiol 80:2836-2847.
55. A receptors underlies potentiation at hippocampal inhibitory synapses. Nature 395:172-177.
56. Obenaus A, Esclapez M, Houser CR (1993) Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures. J Neurosci 13:4470-4485.
57. Okazaki MM, Evenson DA, Nadler JV (1995) Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin. J Comp Neurol 352:515-534.
58. Okazaki MM, Molnár P, Nadler JV (1999) Recurrent mossy fiber pathway in rat dentate gyrus: synaptic currents evoked in presence and absence of seizure-induced growth. J Neurophysiol 81:1645-1660.
59. Otis TS, De Koninck Y, Mody I (1994) Lasting potentiation of inhibition is associated with an increased number of γ-aminobutyric acid type A receptors activated during miniature inhibitory postsynaptic currents. Proc Natl Acad Sci USA 91:7698-7702.
60. Patrylo PR, Schweitzer JS, Dudek FE (1999) Abnormal responses to perforant path stimulation in the dentate gyrus of slices from rats with kainate-induced epilepsy and mossy fiber reorganization. Epilepsy Res 36:31-42.
61. Represa A, Jorquera I, Le Gal La Salle G, Ben-Ari Y (1993) Epilepsy induced collateral sprouting of hippocampal mossy fibers: does it induce the development of ectopic synapses with granule cell dendrites? Hippocampus 3:257-268.
62. Ribak CE, Tran PH, Spigelman I, Okazaki MM, Nadler JV (2000) Status epilepticus-induced hilar basal dendrites on rodent granule cells contribute to recurrent excitatory circuitry. J Comp Neurol 428:240-253.
63. Schwarzer C, Williamson JM, Lothman EW, Vezzani A, Sperk G (1995) Somatostatin, neuropeptide Y, neurokinin B and cholecystokinin immunoreactivity in two chronic models of temporal lobe epilepsy. Neuroscience 69:831-845.
64. Scotti AL, Bollag O, Kalt G, Nitsch C (1997) Loss of perikaryal parvalbumin immunoreactivity from surviving GABAergic neurons in the CA1 field of epileptic gerbils. Hippocampus 7:524-535.
65. Shinoda H, Nadi NS, Schwartz JP (1991) Alterations in somatostatin and proenkephalin mRNA in response to a single amygdaloid stimulation vs. kindling. Mol Brain Res 11:221-226.
66. Simmons ML, Terman GW, Chavkin C (1997) Spontaneous excitatory currents and κ-opioid receptor inhibition in dentate gyrus are increased in the rat pilocarpine model of temporal lobe epilepsy. J Neurophysiol 78:1860-1868.
67. Sloviter RS (1991) 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.
68. Soltesz I, Smetters DK, Mody I (1995) Tonic inhibition originates from synapses close to the soma. Neuron 14:1273-1283.
69. Spigelman I, Yan X-X, Obenaus A, Lee EY-S, Wasterlain CG, Ribak CE (1998) Dentate granule cells form novel basal dendrites in a rat model of temporal lobe epilepsy. Neuroscience 86:109-120.
70. Sutula T, Zhang P, Lynch M, Sayin U, Golarai G, Rod R (1998) Synaptic and axonal remodeling of mossy fibers in the hilus and supragranular region of the dentate gyrus in kainate-treated rats. J Comp Neurol 390:578-594.
71. 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 277:79-90.
72. Turski WA, Cavalheiro EA, Schwarz M, Czuczwar SJ, Kleinrok Z, Turski L (1983) Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav Brain Res 9:315-336.
73. B receptor-mediated responses in GABAergic projection neurons of rat nucleus reticularis thalami in vitro. J Physiol (Lond) 493:845-854.
74. Uruno K, O'Connor MJ, Masukawa LM (1995) Effects of bicuculline and baclofen on paired-pulse depression in the dentate gyrus of epileptic patients. Brain Res 695:163-172.
75. Wanscher B, Kragh J, Barry DI, Bolwig T, Zimmer J (1990) Increased somatostatin and enkephalin-like immunoreactivity in the rat hippocampus following hippocampal kindling. Neurosci Lett 188:33-36.
76. Wierenga CJ, Wadman WJ (1999) Miniature inhibitory postsynaptic currents in CA1 pyramidal neurons after kindling epileptogenesis. J Neurophysiol 82:1352-1362.
77. Williamson A, Spencer SS, Spencer DD (1995) Depth electrode studies and intracellular dentate granule cell recordings in temporal lobe epilepsy. Ann Neurol 38:778-787.
78. Williamson A, Patrylo PR, Spencer DD (1999) Decrease in inhibition in dentate granule cells from patients with temporal lobe epilepsy. Ann Neurol 45:92-99.
79. Wilson CL, Khan SU, Engel Jr I, Isokawa M, Babb TL, Behnke EJ (1998) Paired pulse suppression and facilitation in human epileptogenic hippocampal formation. Epilepsy Res 31:211-230.
80. Wittner L, Maglóczky Z, Borhegyi Z, Halász P, Tóth S, Eróss L, Szabó Z, Freund TF (2001) Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus. Neuroscience 108:587-600.
81. Wuarin J-P, Dudek FE (2001) Excitatory synaptic input to granule cells increases with time after kainate treatment. J Neurophysiol 85:1067-1077.