Lamina-specific changes in hippocampal GABAA/cBZR and mossy fibre sprouting during and following amygdala kindling in the rat

Neurobiology of Disease

Volumn 35, Issue 3, 2009, Pages 337-347

  Liu, David S H ^a   O'Brien, Terence J ^a   Williams, David A ^a   Hicks, Rodney J ^b   Myers, Damian E ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

Epileptogenesis; Flumazenil; GABAA receptor; Hippocampus; Kindling; Mossy fibre sprouting

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BENZODIAZEPINE RECEPTOR; FLUMAZENIL; TRITIUM;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BINDING AFFINITY; BRAIN REGION; CONTROLLED STUDY; DENTATE GYRUS; DISEASE COURSE; DISEASE MODEL; DOWN REGULATION; EPILEPTOGENESIS; HIPPOCAMPUS; KINDLING; MALE; MOSSY FIBER; NERVE SPROUTING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; RECEPTOR AFFINITY; RECEPTOR BINDING; RECEPTOR DENSITY; TEMPORAL LOBE EPILEPSY; TIME; UPREGULATION;

AMYGDALA; ANIMALS; AUTORADIOGRAPHY; CELL COUNT; CELL DEATH; ELECTRIC STIMULATION; ELECTRODES, IMPLANTED; EPILEPSY; FLUMAZENIL; HIPPOCAMPUS; KINDLING, NEUROLOGIC; MALE; NEURONS; RANDOM ALLOCATION; RATS; RATS, WISTAR; RECEPTORS, GABA-A; SEIZURES; TIME FACTORS; TRITIUM;

EID: 68249141781     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2009.05.009     Document Type: Article

References (61)

1. Amaral D., and Witter M. Hippocampal formation. In: Paxinos G. (Ed). The Rat Nervous System. Second Edition (1995), Academic Press, Sydney 443-485
2. Bergersen L., Ruiz A., Bjaalie J.G., Kullmann D.M., and Gundersen V. GABA and GABAA receptors at hippocampal mossy fibre synapses. Eur. J. Neurosci. 18 (2003) 931-941
3. Blair R.E., Sombati S., Lawrence D.C., McCay B.D., and DeLorenzo R.J. Epileptogenesis causes acute and chronic increases in GABAA receptor endocytosis that contributes to the induction and maintenance of seizures in the hippocampal culture model of acquired epilepsy. J. Pharmacol. Exp. Ther. 310 (2004) 871-880
4. Brandt C., Ebert U., and Loscher W. Epilepsy induced by extended amygdala-kindling in rats: lack of clear association between development of spontaneous seizures and neuronal damage. Epilepsy Res. 62 (2004) 135-156
5. Burnham W.M., Niznik H.B., Okazaki M.M., and Kish S.J. Binding of [3H]flunitrazepam and [3H]Ro5-4864 to crude homogenates of amygdala-kindled rat brain: two months post-seizure. Brain Res. 279 (1983) 359-362
6. Cavazos J.E., and Sutula T.P. Progressive neuronal loss induced by kindling: a possible mechanism for mossy fiber synaptic reorganization and hippocampal sclerosis. Brain Res. 527 (1990) 1-6
7. Cavazos J.E., Golarai G., and Sutula T.P. Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence. J. Neurosci. 11 (1991) 2795-2803
8. Cavazos J.E., Das I., and Sutula T.P. Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J. Neurosci. 14 (1994) 3106-3121
9. Clark M., Massenburg G.S., Weiss S.R., and Post R.M. Analysis of the hippocampal GABAA receptor system in kindled rats by autoradiographic and in situ hybridization techniques: contingent tolerance to carbamazepine. Brain Res. Mol. Brain Res. 26 (1994) 309-319
10. Danscher G., Juhl S., Stoltenberg M., Krunderup B., Schroder H.D., and Andreasen A. Autometallographic silver enhancement of zinc sulfide crystals created in cryostat sections from human brain biopsies: a new technique that makes it feasible to demonstrate zinc ions in tissue sections from biopsies and early autopsy material. J. Histochem. Cytochem. 45 (1997) 1503-1510
11. Eghbali M., Curmi J.P., Birnir B., and Gage P.W. Hippocampal GABA(A) channel conductance increased by diazepam. Nature 388 (1997) 71-75
12. Franco-Pons N., Casanovas-Aguilar C., Arroyo S., Rumia J., Perez-Clausell J., and Danscher G. Zinc-rich synaptic boutons in human temporal cortex biopsies. Neuroscience 98 (2000) 429-435
13. Gerfen C.R. Basic neuroanatomical methods. Curr. Protoc. Neurosci. 1 (2003) Chapter 1, Unit 1
14. Goddard G.V., McIntyre D.C., and Leech C.K. A permanent change in brain function resulting from daily electrical stimulation. Exp. Neurol. 25 (1969) 295-330
15. Goodkin H.P., Sun C., Yeh J.L., Mangan P.S., and Kapur J. GABA(A) receptor internalization during seizures. Epilepsia 5 48 Suppl (2007) 109-113
16. Gutiérrez R. Activity-dependent expression of simultaneous glutamatergic and GABAergic neurotransmission from the mossy fibers in vitro. J. Neurophysiol. 87 (2002) 2562-2570
17. Gutiérrez R. The GABAergic phenotype of the "glutamatergic" granule cells of the dentate gyrus. Prog. Neurobiol. 71 (2003) 337-358
18. Hablitz J.J., Tehrani M.H., and Barnes Jr. E.M. Chronic exposure of developing cortical neurons to GABA down-regulates GABA/benzodiazepine receptors and GABA-gated chloride currents. Brain Res. 501 (1989) 332-338
19. Hammers A., Koepp M.J., Hurlemann R., Thom M., Richardson M.P., Brooks D.J., and Duncan J.S. Abnormalities of grey and white matter [11C]flumazenil binding in temporal lobe epilepsy with normal MRI. Brain 125 (2002) 2257-2271
20. Hand K.S., Baird V.H., Van Paesschen W., Koepp M.J., Revesz T., Thom M., Harkness W.F., Duncan J.S., and Bowery N.G. Central benzodiazepine receptor autoradiography in hippocampal sclerosis. Br. J. Pharmacol. 122 (1997) 358-364
21. Hansen A., Jorgensen O.S., Bolwig T.G., and Barry D.I. Hippocampal kindling in the rat is associated with time-dependent increases in the concentration of glial fibrillary acidic protein. J. Neurochem. 57 (1991) 1716-1720
22. Henry T.R., Frey K.A., Sackellares J.C., Gilman S., Koeppe R.A., Brunberg J.A., Ross D.A., Berent S., Young A.B., and Kuhl D.E. In vivo cerebral metabolism and central benzodiazepine-receptor binding in temporal lobe epilepsy. Neurology 43 1998-2006 (1993)
23. Jaarsma D., and Korf J. A novel non-perfusion Timm method for human brain tissue. J. Neurosci. Methods 35 (1990) 125-131
24. Jaffe D.B., and Gutiérrez R. Mossy fiber synaptic transmission: communication from the dentate gyrus to area CA3. Prog. Brain Res. 163 (2007) 109-132
25. Kamphuis W., Gorter J.A., Wadman W.J., and Lopes da Silva F.H. 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 (1992) 101-105
26. Kamphuis W., De Rijk T.C., and Lopes da Silva F.H. GABAA receptor beta 1-3 subunit gene expression in the hippocampus of kindled rats. Neurosci. Lett. 174 (1994) 5-8
27. Kamphuis W., De Rijk T.C., and Lopes da Silva F.H. Expression of GABAA receptor subunit mRNAs in hippocampal pyramidal and granular neurons in the kindling model of epileptogenesis: an in situ hybridization study. Brain Res. Mol. Brain Res. 31 (1995) 33-47
28. Koepp M.J., Labbe C., Richardson M.P., Brooks D.J., Van Paesschen W., Cunningham V.J., and Duncan J.S. Regional hippocampal [11C]flumazenil PET in temporal lobe epilepsy with unilateral and bilateral hippocampal sclerosis. Brain 120 Pt 10 (1997) 1865-1876
29. Korpi E.R., Grunder G., and Luddens H. Drug interactions at GABA(A) receptors. Prog. Neurobiol. 67 (2002) 113-159
30. Lamas M., Gomez-Lira G., and Gutiérrez R. Vesicular GABA transporter mRNA expression in the dentate gyrus and in mossy fiber synaptosomes. Brain Res. Mol. Brain Res. 93 (2001) 209-214
31. Lothman E.W., Stringer J.L., and Bertram E.H. The dentate gyrus as a control point for seizures in the hippocampus and beyond. Epilepsy. Res. Suppl. 7 (1992) 301-313
32. Maru E., and Goddard G.V. Alteration in dentate neuronal activities associated with perforant path kindling. III Enhancement of synaptic inhibition. Exp. Neurol. 96 (1987) 46-60
33. McDonald J.W., Garofalo E.A., Hood T., Sackellares J.C., Gilman S., McKeever P.E., Troncoso J.C., and Johnston M.V. Altered excitatory and inhibitory amino acid receptor binding in hippocampus of patients with temporal lobe epilepsy. Ann. Neurol. 29 (1991) 529-541
34. McLeod M., Pralong D., Copolov D., and Dean B. [(3)H]Flumazenil binding in the human hippocampal formation, frontal cortex and cerebellum detected by high-resolution phosphorimaging. Brain Res. 926 (2002) 27-32
35. McNamara J.O. Kindling model of epilepsy. Adv. Neurol. 44 (1986) 303-318
36. McNamara J.O., Peper A.M., and Patrone V. Repeated seizures induce long-term increase in hippocampal benzodiazepine receptors. Proc. Natl. Acad. Sci. U. S. A. 77 (1980) 3029-3032
37. Möhler H., and Richards J.G. Agonist and antagonist benzodiazepine receptor interaction in vitro. Nature 294 (1981) 763-765
38. Nishimura T., Schwarzer C., Gasser E., Kato N., Vezzani A., and Sperk G. Altered expression of GABA(A) and GABA(B) receptor subunit mRNAs in the hippocampus after kindling and electrically induced status epilepticus. Neuroscience 134 (2005) 691-704
39. Nobrega J.N., Kish S.J., and Burnham W.M. Autoradiographic analysis of benzodiazepine binding in entorhinal-kindled rat brains. Brain Res. 498 (1989) 315-322
40. Nusser Z., Hajos N., Somogyi P., and Mody I. Increased number of synaptic GABA(A) receptors underlies potentiation at hippocampal inhibitory synapses. Nature 395 (1998) 172-177
41. Okun F., Weizman R., Katz Y., Bomzon A., Youdim M.B., and Gavish M. Increase in central and peripheral benzodiazepine receptors following surgery. Brain Res. 458 (1988) 31-36
42. Otis T.S., De Koninck Y., and Mody I. Lasting potentiation of inhibition is associated with an increased number of gamma-aminobutyric acid type A receptors activated during miniature inhibitory postsynaptic currents. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 7698-7702
43. Paxinos, G., Watson, C., 1998. The Rat Brain in stereotaxic coordinates, fourth ed. Academic Press, San Diego.
44. Racine R.J. Modification of seizure activity by electrical stimulation. II Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32 (1972) 281-294
45. Ramirez M., and Gutiérrez R. Activity-dependent expression of GAD67 in the granule cells of the rat hippocampus. Brain Res. 917 (2001) 139-146
46. Represa A., Le Gall La Salle G., and Ben-Ari Y. Hippocampal plasticity in the kindling model of epilepsy in rats. Neurosci. Lett. 99 (1989) 345-350
47. Rossler A.S., Launay J.M., Venault P., Dodd R.H., and Chapouthier G. Changes in benzodiazepine binding in a subkindling situation. Epilepsia 41 (2000) 651-654
48. Sata Y., Matsuda K., Mihara T., Aihara M., Yagi K., and Yonekura Y. Quantitative analysis of benzodiazepine receptor in temporal lobe epilepsy: [(125)I]iomazenil autoradiographic study of surgically resected specimens. Epilepsia 43 (2002) 1039-1048
49. Schwartz R.D. The GABAA receptor-gated ion channel: biochemical and pharmacological studies of structure and function. Biochem. Pharmacol. 37 (1988) 3369-3375
50. Shin C., Pedersen H.B., and McNamara J.O. gamma-Aminobutyric acid and benzodiazepine receptors in the kindling model of epilepsy: a quantitative radiohistochemical study. J Neurosci. 5 (1985) 2696-2701
51. Sloviter R.S., Dichter M.A., Rachinsky T.L., Dean E., Goodman J.H., Sollas A.L., and Martin D.L. Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J. Comp. Neurol. 373 (1996) 593-618
52. Spiller A.E., and Racine R.J. The effect of kindling beyond the 'stage 5' criterion on paired-pulse depression and hilar cell counts in the dentate gyrus. Brain Res. 635 (1994) 139-147
53. Sutula T., He X.X., Cavazos J., and Scott G. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 239 (1988) 1147-1150
54. Tehrani M.H., and Barnes Jr. E.M. Agonist-dependent internalization of gamma-aminobutyric acidA/benzodiazepine receptors in chick cortical neurons. J. Neurochem. 57 (1991) 1307-1312
55. Titulaer M.N., Kamphuis W., Pool C.W., van Heerikhuize J.J., and Lopes da Silva F.H. Kindling induces time-dependent and regional specific changes in the [3H]muscimol binding in the rat hippocampus: a quantitative autoradiographic study. Neuroscience 59 (1994) 817-826
56. Titulaer M.N., Kamphuis W., and Lopes da Silva F.H. Long-term and regional specific changes in [3H]flunitrazepam binding in kindled rat hippocampus. Neuroscience 68 (1995) 399-406
57. Tuff L.P., Racine R.J., and Adamec R. The effects of kindling on GABA-mediated inhibition in the dentate gyrus of the rat. I Paired-pulse depression. Brain Res. 277 (1983) 79-90
58. Tuff L.P., Racine R.J., and Mishra R.K. The effects of kindling on GABA-mediated inhibition in the dentate gyrus of the rat. II Receptor binding. Brain Res. 277 (1983) 91-98
59. Van der Zee C.E., Rashid K., Le K., Moore K.A., Stanisz J., Diamond J., Racine R.J., and Fahnestock M. Intraventricular administration of antibodies to nerve growth factor retards kindling and blocks mossy fiber sprouting in adult rats. J. Neurosci. 15 (1995) 5316-5323
60. Walker M.C., Ruiz A., and Kullmann D.M. Do mossy fibers release GABA?. Epilepsia 5 43 Suppl (2002) 196-202
61. West M.J., Slomianka L., and Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231 (1991) 482-497