Vulnerability of the dentate gyrus to aging and intracerebroventricular administration of kainic acid

Experimental Neurology

Volumn 158, Issue 2, 1999, Pages 491-503

  Shetty, Ashok K ^a   Turner, Dennis A ^a  

^a NONE

Author keywords

Aging; Dentate granule cells; Dentate gyrus; Dentate hilar cells; Excitotoxic lesions; Kainic acid

Indexed keywords

KAINIC ACID;

ADOLESCENT; AGED; AGING; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DENTATE GYRUS; GRANULE CELL; HIPPOCAMPUS; LATERAL BRAIN VENTRICLE; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0032838951     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1999.7107     Document Type: Article

References (67)

1. Adams B., Sazgar M., Osehobo P., Van der Zee C. E. E. M., Diamond J., Fahnestock M., Racine R. J. Nerve growth factor accelerates seizure development, enhances mossy fiber sprouting, and attenuates seizure-induced decreases in neuronal density in the kindling model of epilepsy. J. Neurosci. 17:1997;5288-5296.
2. Amaral D. G. A Golgi study of the cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 182:1978;851-914.
3. Amaral D. G., Witter M. P. Hippocampal formation. Paxinos G. The Rat Nervous System. 1995;443-493 Academic Press, London.
4. Anderson K. J., Scheff S. W., Dekosky S. T. Reactive synaptogenesis in hippocampal area CA1 of aged and young adult rats. J. Comp. Neurol. 252:1986;374-384.
5. Bakst I., Avenano C., Morrison J. H., Amaral D. G. An experimental analysis of the origins of somatostatin-immunoreactivity in the dentate gyrus of the rat. J. Neurosci. 6:1986;1452-1462.
6. Beal M. F. Mechanisms of excitotoxicity in neurologic diseases. FASEB J. 6:1992;3338-3344.
7. Ben-Ari Y. Limbic seizures and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy. Neuroscience. 14:1985;375-403.
8. Ben-Ari Y., Represa A. Brief seizure episodes induce long term potentiation and mossy fiber sprouting in the hippocampus. Trends Neurosci. 13:1990;312-318.
9. Bertram E. H., Lothman E. W. Morphometric effects of intermittent kindled seizures and limbic status epilepticus in the dentate gyrus of the rat. Brain Res. 603:1993;25-31.
10. Blackstad T. W. Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J. Comp. Neurol. 105:1956;417-537.
11. Carpenter M. K., Parker I., Miledi R. Messenger RNAs coding for receptors and channels in the cerebral cortex of adult and aged rats. Mol. Brain Res. 13:1992;1-5.
12. Choi D. W. Excitotoxic cell death. J. Neurobiol. 23:1992;1261-1276.
13. Clark A. S., Magnusson K. R., Cotman C. W. In vitro autoradiography of hippocampal excitatory amino acid binding in aged Fischer 344 rats: relationship to performance on the Morris water maze. Behav. Neurosci. 106:1992;324-335.
14. Cotman C. W., Nieto S. M. Progress in facilitating the recovery of function after central nervous system trauma. Ann. N. Y. Acad. Sci. 457:1985;83-104.
15. Cronin J. A., Dudek F. E. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res. 474:1988;181-184.
16. Dawson R. J., Wallace D. R. Kainic acid induced seizures in aged rats: Neurochemical correlates. Brain Res. Bull. 29:1992;459-468.
17. DeToledo-Morrell L., Geinisman Y., Morrel F. Age-dependent alterations in hippocampal synaptic plasticity: Relation to memory disorders. Neurobiol. Aging. 9:1988;581-590.
18. DeToledo-Morrell L., Morrell F. Alzheimer's disease: New developments for noninvasive detection of early cases. Curr. Opin. Neurol. Neurosurg. 6:1988;113-118.
19. Deupree D. L., Bradley J., Turner D. A. Age-related alterations in potentiation in the CA1 region in F344 rats. Neurobiol. Aging. 14:1993;249-258.
20. Finch C. E. Neuron atrophy during aging: programmed or sporadic. Trends Neurosci. 16:1993;104-110.
21. Freund T. F., Magloczky Z. Early degeneration of calretinin containing neurons in rat hippocampus after ischemia. Neuroscience. 565:1993;581-596.
22. Frotscher M., Seress L., Schwerdtfeger, Buhl E. The mossy cells of the fascia dentata: A comparative study of their fine structure and synaptic connections in rodents and primates. J. Comp. Neurol. 312:1991;145-163.
23. Frotscher M., Zimmer J. Commissural fibers terminated on non-pyramidal neurons in the guinea pig hippocampus - a combined Golgi/EM degeneration study. Brain Res. 265:1983;289-293.
24. Gage F. H., Kelly P. A., Bjorklund A. Regional changes in glucose metabolism reflect cognitive impairments in aged rats. J. Neurosci. 4:1984;2856-2865.
25. Geddes J. W., Monaghan D. T., Cotman C. W., Lott I. T., Kim R. C., Chui H. C. Plasticity of hippocampal circuitry in Alzheimer's disease. Science. 225:1985;1179-1181.
26. Geinisman Y., DeToledo-Morrel L., Morrel F. Loss of perforated synapses in the dentate gyrus: Morphological substrate of memory deficit in aged rats. Proc. Natl. Acad. Sci. USA. 83:1986;3027-3031.
27. Halasy K., Somogyi P. Subdivisions in the multiple GABAergic innervation of granule cells in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 5:1993;411-429.
28. Haug F.-M. S. Light microscopical mapping of the hippocampal region, the pyriform cortex and the corticomedial amygdaloid nuclei of the rat with Timm's sulfide silver method. I. Area dentata, hippocampus and subiculum. Z. Anat. Entwickl. Gesch. 145:1974;1-27.
29. Holtzman D. M., Lowenstein D. H. Selective inhibition of axon outgrowth by antibodies to NGF in a model of temporal lobe epilepsy. J. Neurosci. 15:1995;7062-7070.
30. Kadar T., Silbermann M., Bradeis R., Levy A. Age-related structural changes in the rat hippocampus: Correlation with working memory deficiency. Brain Res. 512:1990;113-120.
31. Kerr D. S., Campbell L. W., Thibault O., Landfield P. W. Hippocampal glucocorticoid receptor activation enhances voltage-dependent Ca++ conductances: Relevance to brain aging. Proc. Natl. Acad. Sci. USA. 89:1992;8257-8531.
32. Kesslak J. P., Yuan D., Neeper S., Cotman C. W. Vulnerability of the hippocampus to kainate excitotoxicity in the aged, mature and young adult rat. Neurosci. Lett. 188:1995;117-120.
33. Kishi K., Stanfield B. B., Cowan W. M. A quantitative EM autoradiographic study of the commissural and associational connections of the dentate gyrus in the rat. Anat. Embryol. 160:1980;173-186.
34. Laatsch R. H., Cowan W. M. Electron microscopic studies of the dentate gyrus of the rat. I. Normal structure with special reference to synaptic organization. J. Comp. Neurol. 128:1966;359-396.
35. Laatsch R. H., Cowan W. M. Electron microscopic studies of the dentate gyrus of the rat. II. Degeneration of commissural afferents. J. Comp. Neurol. 130:1967;241-262.
36. Landfield P. W., Thibault O., Mazzanti M. L., Porter N. M., Kerr D. S. Mechanisms of neuronal death in brain aging and Alzheimer's disease: Role of endocrine-mediated calcium dyshomeostasis. J. Neurobiol. 23:1992;1247-1260.
37. Laurberg S. Commissural and intrinsic connections of the rat hippocampus. J. Comp. Neurol. 184:1979;685-708.
38. Laurberg S., Sorensen K. E. Associational and commissural collaterals of neurons in the hippocampal formation (hilus fasciae dentatae and subfield ca3). Brain Res. 212:1981;287-300.
39. Mathern G. W., Cifuentes F., Leite J. P., Pretorius J. K., Babb T. L. Hippocampal EEG excitability and chronic spontaneous seizures are associated with aberrant synaptic reorganization in the rat intrahippocampal kainate model. Electroencephalogr. Clin. Neurophysiol. 87:1993;326-339.
40. McWilliams J. R., Lynch G. Synaptic density and axonal sprouting in rat hippocampus: Stability in adulthood and decline in late adult hood. Brain Res. 294:1984;152-156.
41. Mello L. E. A. M., Cavelheiro E. A., Tan A. M., Kupfer W. R., Pretorius J. K., Babb T. L., Finch D. M. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: Cell loss and mossy fiber sprouting. Epilepsia. 34:1993;985-995.
42. Nadler J. V., Perry B. W., Cotman C. W. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature. 271:1978;676-677.
43. Nadler J. V., Perry B. W., Gentry C., Cotman C. W. Degeneration of hippocampal CA3 pyramidal cells induced by intraventricular kainic acid. J. Comp. Neurol. 192:1980;333-359.
44. Nadler J. V., Perry B. W., Cotman C. W. Selective reinnervation of hippocampal area CA1 and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res. 182:1980;1-9.
45. Nadler J. V., Evenson D. A., Smith E. M. Evidence from lesion studies for epileptogenic and non-epileptogenic neurotoxic interactions between kainic acid and excitatory innervation. Brain Res. 205:1981;405-410.
46. Okazaki M. M., Evenson D. A., Nadler J. V. Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: Visualization after retrograde transport of biocytin. J. Comp. Neurol. 352:1995;515-534.
47. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. 1986;Academic Press, London.
48. Pisa M., Sanberg P. R., Corcoran M. E., Fibiger H. C. Spontaneously recurrent seizures after intracerebral injections of kainic acid in rat: a possible model of temporal lobe epilepsy. Brain Res. 200:1980;481-487.
49. Rapp P. R., Amaral D. G. Individual differences in the cognitive and neurobiological consequences of normal aging. Trends Neurosci. 15:1992;340-345.
50. Rasmussen T., Schliemann T., Sorensen J. C., Zimmer J., West M. J. Memory impaired rats: No loss of principal hippocampal and subicular neurons. Neurobiol. Aging. 17:1996;143-147.
51. Ribak C. E., Seress L., Amaral D. G. The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus. J. Neurocytol. 14:1985;835-857.
52. Scharfman H. E., Kunkel D. D., Schwartzkroin P. A. Synaptic connections of dentate granule cells and hilar neurons: Results of paired intracellular recordings and intracellular horseradish peroxidase injections. Neuroscience. 37:1990;693-707.
53. Shetty A. K., Turner D. A. Enhanced cell survival in fetal hippocampal suspension transplants grafted to adult rat hippocampus following kainate lesions: A three-dimensional graft reconstruction study. Neuroscience. 67:1995;561-582.
54. Shetty A. K., Turner D. A. Intracerebroventricular administration of kainic acid in rats causes alterations in hippocampal calbindin and non-phosphorylated neurofilament protein expression. J. Comp. Neurol. 363:1995;581-599.
55. Shetty A. K., Turner D. A. Non-phosphorylated neurofilament protein immunoreactivity in adult and developing rat hippocampus: Specificity and application in grafting studies. Brain Res. 676:1995;293-306.
56. Shetty A. K., Turner D. A. Development of fetal hippocampal grafts in intact and lesioned hippocampus. Prog. Neurobiol. 50:1996;593-653.
57. Shetty A. K., Turner D. A. Development of long-distance efferent projections from fetal hippocampal grafts depends upon pathway specificity and graft location in kainate-lesioned adult hippocampus. Neuroscience. 76:1997;1205-1219.
58. Shetty A. K., Turner D. A. Fetal hippocampal cells grafted to kainate-lesioned CA3 of adult hippocampus suppress aberrant supragranular sprouting of host mossy fibers. Exp. Neurol. 143:1997;231-245.
59. Shetty A. K., Turner D. A. Hippocampal interneurons expressing glutamic acid decarboxylase and calcium binding proteins decrease with aging in Fischer 344 rats. J. Comp. Neurol. 394:1998;252-269.
60. Sperk G. Kainic acid seizures in the rat. Prog. Neurobiol. 42:1994;1-32.
61. Swanson L. W., Wyss J. M., Cowan W. M. An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J. Comp. Neurol. 181:1978;681-716.
62. Swanson L. W., Sawchenko P. E., Cowan W. M. Evidence for collateral projections by neurons in ammon's horn, the dentate gyrus, and the subiculum: A multiple retrograde labeling study in the rat. J. Neurosci. 1:1981;548-559.
63. Tauck D. L., Nadler J. V. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid treated rats. J. Neurosci. 4:1985;1016-1022.
64. Tortosa A., Ferrer I. Parvalbumin immunoreactivity in the hippocampus of the gerbil after transient forebrain ischemia: A qualitative and quantitative sequential study. Neuroscience. 55:1993;33-43.
65. Turner D. A., Wheal H. V. Excitatory synaptic potentials in kainic acid denervated rat CA1 pyramidal neurons. J. Neurosci. 11:1991;2786-2794.
66. Wozniak D. F., Stewart G. R., Miller J. P., Olney J. W. Age-related sensitivity to kainate neurotoxicity. Exp. Neurol. 114:1991;250-253.
67. Zimmer J. Ipsilateral afferents to the commissural zone of the fascia dentata, demonstrated in decommissurated rats by silver impregnation. J. Comp. Neurol. 142:1971;393-416.