Selective loss of dentate hilar interneurons contributes to reduced synaptic inhibition of granule cells in an electrical stimulation-based animal model of temporal lobe epilepsy

Journal of Comparative Neurology

Volumn 500, Issue 5, 2007, Pages 876-893

  Sun, Chengsan ^a   Mtchedlishvili, Zakaria ^a   Bertram, Edward H ^a   Erisir, Alev ^a   Kapur, Jaideep ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Colocalization; Neuropeptide Y; Somatostatin; Status epilepticus

Indexed keywords

4 AMINOBUTYRIC ACID; CHOLECYSTOKININ; FLUORESCENT DYE; FLUORO JADE B; NEUROPEPTIDE; NEUROPEPTIDE Y; PARVALBUMIN; SOMATOSTATIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DENTATE GYRUS; ELECTRON MICROSCOPY; ELECTROSTIMULATION; EPILEPTIC STATE; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MALE; NERVE CELL DEGENERATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SYNAPSE; SYNAPTIC INHIBITION; TEMPORAL LOBE EPILEPSY;

ANIMALS; CHOLECYSTOKININ; DENTATE GYRUS; ELECTRIC STIMULATION; EPILEPSY, TEMPORAL LOBE; FLUORESCENT DYES; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MALE; MATCHED-PAIR ANALYSIS; NERVE DEGENERATION; NEUROPEPTIDE Y; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SOMATOSTATIN; SYNAPTIC TRANSMISSION;

EID: 33846368408     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21207     Document Type: Article

References (64)

1. Bekenstein JW, Lothman EW. 1993. Dormancy of inhibitory interneurons in a model of temporal lobe epilepsy. Science 259:97-100.
2. Bender RA, Soleymani SV, Brewster AL, Nguyen ST, Beck H, Mathern GW, Baram TZ. 2003. Enhanced expression of a specific hyperpolarization-activated cyclic nucleotide-gated cation channel (HCN) in surviving dentate gyrus granule cells of human and experimental epileptic hippocampus. J Neurosci 23:6826-6836.
3. Bertram EH, Cornett J. 1993. The ontogeny of seizures in a rat model of limbic epilepsy: evidence for a kindling process in the development of chronic spontaneous seizures. Brain Res 625:295-300.
4. Bertram EH, Williamson JM, Cornett JF, Spradlin S, Chen ZF. 1997. Design and construction of a long-term continuous video-EEG monitoring unit for simultaneous recording of multiple small animals. Brain Res Brain Res Protoc 2:85-97.
5. 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.
6. Celio MR. 1990. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475.
7. Chan-Palay V, Kohler C, Haesler U, Lang W, Yasargil G. 1986. Distribution of neurons and axons immunoreactive with antisera against neuropeptide Y in the normal human hippocampus. J Comp Neurol 248:360-375.
8. 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.
9. Coulter DA. 2001. Epilepsy-associated plasticity in gamma-aminobutyric acid receptor expression, function, and inhibitory synaptic properties. Int Rev Neurobiol 45:237-252.
10. Del Castillo J, Katz B. 1956. Biophysical aspects of neuromuscular transmission. Prog Biophys Biophys Chem 6:121-170.
11. 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.
12. Deller T, Leranth C. 1990. Synaptic connections of neuropeptide Y (NPY) immunoreactive neurons in the hilar area of the rat hippocampus. J Comp Neurol 300:433-447.
13. Esclapez M, Houser CR. 1995. Somatostatin neurons are a subpopulation of GABA neurons in the rat dentate gyrus: evidence from colocalization of pre-prosomatostatin and glutamate decarboxylase messenger RNAs. Neuroscience 64:339-355.
14. Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6:347-470.
15. Fujikawa DG. 1996. The temporal evolution of neuronal damage from pilocarpine-induced status epilepticus. Brain Res 725:11-22.
16. A receptor funcction in dentate granule and CA1 neurons. J Neurophysiol 77:1924-1938.
17. Heck WL, Slusarczyk A, Basaraba AM, Schweitzer L. 2002. Subcellular localization of GABA receptors in the central nervous system using post-embedding immunohistochemistry. Brain Res Brain Res Protoc 9:173-180.
18. 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.
19. Ingram SM, Krause RG, Baldino F Jr, Skeen LC, Lewis ME. 1989. Neuronal localization of cholecystokinin mRNA in the rat brain by using in situ hybridization histochemistry. J Comp Neurol 287:260-272.
20. Innis RB, Correa FM, Uhl GR, Schneider B, Snyder SH. 1979. Cholecystokinin octapeptide-like immunoreactivity: histochemical localization in rat brain. Proc Natl Acad Sci U S A 76:521-525.
21. Jakab RL, Bowyer JF. 2002. Parvalbumin neuron circuits and microglia in three dopamine-poor cortical regions remain sensitive to amphetamine exposure in the absence of hyperthermia, seizure and stroke. Brain Res 958:52-69.
22. 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.
23. Kobayashi M, Buckmaster PS. 2003. Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J Neurosci 23:2440-2452.
24. Kohler C, Eriksson LG, Davies S, Chan-Palay V. 1987. Co-localization of neuropeptide tyrosine and somatostatin immunoreactivity in neurons of individual subfields of the rat hippocampal region. Neurosci Lett 78:1-6.
25. 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.
26. Leroy C, Poisbeau P, Keller AF, Nehlig A. 2004. Pharmacological plasticity of GABA(A) receptors at dentate gyrus synapses in a rat model of temporal lobe epilepsy. J Physiol 557:473-487.
27. Lothman EW, Bertram EH, Bekenstein JW, Perlin JB. 1989. Self-sustaining limbic status epilepticus induced by 'continuous' hippocampal stimulation: electrographic and behavioral characteristics. Epilepsy Res 3:107-119.
28. Lothman EW, Bertram EH, Kapur J, Stringer JL. 1990. Recurrent spontaneous hippocampal seizures in the rat as a chronic sequela to limbic status epilepticus. Epilepsy Res 6:110-118.
29. Mangan PS, Bertram EH III. 1998. Ontogeny of altered synaptic function in a rat model of chronic temporal lobe epilepsy. Brain Res 799:183-196.
30. Mathern GW, Babb TL, Pretorius JK, Leite JP. 1995. Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J Neurosci 15:3990-4004.
31. McNamara JO. 1999. Emerging insights into the genesis of epilepsy. Nature 399:A15-A22.
32. Milner TA, Bacon CE. 1989. Ultrastructural localization of somatostatin-like immunoreactivity in the rat dentate gyrus. J Comp Neurol 290:544-560.
33. Mody I. 1998. Ion channels in epilepsy. Int Rev Neurobiol 42:199-226.
34. Mody I, Heinemann U. 1987. NMDA receptors of dentate gyrus granule cells participate in synaptic transmission following kindling. Nature 326:701-704.
35. Mtchedlishvili Z, Bertram EH, Kapur J. 2001. Diminished allopregnanolone enhancement of GABA(A) receptor currents in a rat model of chronic temporal lobe epilepsy. J Physiol 537:453-465.
36. Naus CC, Bloom FE. 1988. Immunohistochemical analysis of the development of somatostatin in the reeler neocortex. Brain Res 471:61-68.
37. Naus CC, Morrison JH, Bloom FE. 1988. Development of somatostatin- containing neurons and fibers in the rat hippocampus. Brain Res 468:113-121.
38. Nusser Z, Hajos N, Somogyi P, Mody I. 1998. Increased number of GABA-A receptors underlies potentiation of hippocampal synapses. Nature 395:172-177.
39. 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.
40. 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 U S A 91:7698-7702.
41. Paxinos G, Watson C. 1998. The Rat Brain in the Stereotaxic Coordinates. Fourth Edition. Academic Press, San Diego, CA.
42. Priestley JV, Rethelyi M, Lund PK. 1991. Semi-quantitative analysis of somatostatin mRNA distribution in the rat central nervous system using in situ hybridization. J Chem Neuroanat 4:131-153.
43. Ribak CE, Harris AB, Vaughn JE, Roberts E. 1979. Inhibitory, GABAergic nerve terminals decrease at sites of focal epilepsy. Science 205:211-214.
44. Ribak CE, Bradburne RM, Harris AB. 1982. A preferential loss of GABAergic, symmetric synapses in epileptic foci: a quantitative ultrastructural analysis of monkey neocortex. J Neurosci 2:1725-1735.
45. Robbins RJ, Brines ML, Kim JH, Adrian T, de Lanerolle N, Welsh S, Spencer DD. 1991. A selective loss of somatostatin in the hippocampus of patients with temporal lobe epilepsy. Ann Neurol 29:325-332.
46. Sayin U, Osting S, Hagen J, Rutecki P, Sutula T. 2003. Spontaneous seizures and loss of axo-axonic and axo-somatic inhibition induced by repeated brief seizures in kindled rats. J Neurosci 23:2759-2768.
47. Schmued LC, Hopkins KJ. 2000. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874:123-130.
48. 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.
49. Seto-Ohshima A, Emson PC, Berchtold MW, Heizmann CW. 1989. Localization of parvalbumin mRNA in rat brain by in situ hybridization histochemistry. Exp Brain Res 75:653-658.
50. Shao LR, Dudek FE. 2005. Changes in mIPSCs and sIPSCs after kainate treatment: evidence for loss of inhibitory input to dentate granule cells and possible compensatory responses. J Neurophysiol 94:952-960.
51. Sloviter RS. 1987. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235:73-76.
52. 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.
53. Sloviter RS. 1992. Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci Lett 137:91-96.
54. Sloviter RS, Nilaver G. 1987. Immunocytochemical localization of GABA-, cholecystokinin-, vasoactive intestinal polypeptide-, and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat. J Comp Neurol 256:42-60.
55. Sloviter RS, Dean E, Sollas AL, Goodman JH. 1996. Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat. J Comp Neurol 366:516-533.
56. Sloviter RS, Ali-Akbarian L, Horvath KD, Menkens KA. 2001. Substance P receptor expression by inhibitory interneurons of the rat hippocampus: enhanced detection using improved immunocytochemical methods for the preservation and colocalization of GABA and other neuronal markers. J Comp Neurol 430:283-305.
57. Sloviter RS, Zappone CA, Harvey BD, Bumanglag AV, Bender RA, Frotscher M. 2003. "Dormant basket cell" hypothesis revisited: relative vulnerabilities of dentate gyrus mossy cells and inhibitory interneurons after hippocampal status epilepticus in the rat. J Comp Neurol 459:44-76.
58. 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 hyperinhibition in chronically epileptic rats. J Comp Neurol 494:944-960.
59. Soltesz I, Smetters DK, Mody I. 1995. Tonic inhibition originates from synapses close to the soma. Neuron 14:1273-1283.
60. Sun C, Sieghart W, Kapur J. 2004. Distribution of alpha1, alpha4, gamma2, and delta subunits of GABAA receptors in hippocampal granule cells. Brain Res 1029:207-216.
61. Tauck DL, Nadler JV. 1985. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5:1016-1022.
62. 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.
63. Vezzani A, Schwarzer C, Lothman EW, Williamson J, Sperk. 1996. Functional changes in somatostatin and neuropeptide Y containing neurons in the rat hippocampus in chronic models of limbic seizures. Epilepsy Res 26:267-279.
64. Wuarin JP, Dudek FE. 1996. Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rats. J Neurosci 16:4438-4448.