Ultrastructural analysis of the progression of neurodegeneration in the septum following fimbria-fornix transection

Neuroscience

Volumn 86, Issue 4, 1998, Pages 1259-1272

  Ginsberg, S D ^a,b   Martin, L J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Axotomy; Cell death; Lateral septal nucleus; Medial septal nucleus; Retrograde degeneration; Synaptic stripping

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FORNIX; BRAIN INJURY; CELL INCLUSION; CELL LOSS; CELL VACUOLE; CONTROLLED STUDY; MALE; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROPIL; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; RAT; SEPTUM NUCLEUS;

ANIMALS; AXONS; AXOTOMY; BRAIN; CELL DEATH; HIPPOCAMPUS; MALE; MICROSCOPY, ELECTRON; NERVE DEGENERATION; NEUROGLIA; NEUROPIL; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0032543714     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00136-5     Document Type: Article

References (66)

1. Alonso J. R., Frotscher M. Hippocampo-septal fibers terminate on identified spiny neurons in the lateral septum: a combined Golgi/electron-microscopic and degeneration study in the rat. Cell Tiss. Res. 258:1989;243-246.
2. Amaral D. G. (1987) Memory: anatomical organization of candidate brain regions. In Handbook of Physiology. Section 1: The Nervous System. V. Higher Functions of the Brain, Part 1 (eds Mountcastle V. B., Plum F. and Geiger S. R.), pp. 211-294. American Physiological Society, Bethesda.
3. Amaral D. G., Kurz J. An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. J. comp. Neurol. 240:1985;37-59.
4. Armstrong D. M., Terry R. D., Deteresa R. M., Bruce G., Hersh L. B., Gage F. H. Response of septal cholinergic neurons to axotomy. J. comp. Neurol. 264:1987;421-436.
5. Barron K. D., Means E. D., Larsen E. Ultrastructure of retrograde degeneration in thalamus of rat. J. Neuropath. exp. Neurol. 32:1973;218-244.
6. Bialowas J., Frotscher M. Choline acetyltransferase-immunoreactive neurons and terminals in the rat septal complex: a combined light and electron microscopic study. J. comp. Neurol. 259:1987;298-307.
7. Blinzinger K., Kreutzberg G. Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Z. Zellforsch. 85:1968;145-157.
8. Caceres A., Steward O. Dendritic reorganization in the denervated dentate gyrus of the rat following entorhinal cortical lesions: a Golgi and electron microscopic analysis. J. comp. Neurol. 214:1983;387-403.
9. Daitz H. M., Powell T. P. S. Studies of the connexions of the fornix system. J. Neurol. Neurosurg. Neuropsychiat. 17:1954;75-82.
10. DeFrance J. F., Shimono T., Kitai S. T. Anatomical distribution of the hippocampal fibers afferent to the lateral septal nucleus. Brain Res. 34:1971;176-180.
11. Field P. M., Raisman G. Relative slowness of heterotypic synaptogenesis in the septal nuclei. Brain Res. 272:1983;83-99.
12. Gage F. H., Wictorin K., Fischer W., Williams L. R., Varon S., Björklund A. Retrograde cell changes in medial septum and diagonal band following fimbria-fornix transection: quantitative temporal analysis. Neuroscience. 19:1986;241-255.
13. Gage F. H., Olejniczak P., Armstrong D. M. Astrocytes are important for sprouting in the septohippocampal circuit. Expl Neurol. 102:1988;2-13.
14. Gaykema R. P. A., Van der Kuil J., Hersh L. B., Luiten P. G. M. Patterns of direct projections from the hippocampus to the medial septum-diagonal band complex: anterograde tracing with Phaseolus vulgaris leucoagglutinin combined with immunohistochemistry of choline acetyltransferase. Neuroscience. 43:1991;349-360.
15. Ginsberg S. D., Martin L. J., Rothstein J. D. Regional deafferentation down-regulates subtypes of glutamate transporter proteins. J. Neurochem. 65:1995;2800-2803.
16. Ginsberg S. D., Rothstein J. D., Price D. L., Martin L. J. Fimbria-fornix transections selectively down-regulate subtypes of glutamate transporter and glutamate receptor proteins in septum and hippocampus. J. Neurochem. 67:1996;1208-1216.
17. Hagg T., Manthorpe M., Vahlsing H. L., Varon S. Delayed treatment with nerve growth factor reverses the apparent loss of cholinergic neurons after acute brain damage. Expl Neurol. 101:1988;303-312.
18. Haas C. A., Deller T., Naumann T., Frotscher M. Selective expression of the immediate early gene c-jun in axotomized rat medial septal neurons is not related to neuronal degeneration. J. Neurosci. 16:1996;1894-1903.
19. Hefti F. Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J. Neurosci. 6:1986;2155-2162.
20. Jakab R. L., Leranth C. Somatospiny neurons in the rat lateral septal area are synaptic targets of hippocamposeptal fibers: a combined EM/Golgi and degeneration study. Synapse. 6:1990;10-22.
21. Joëls M., Urban I. J. A. Electrophysiological and pharmacological evidence in favor of amino acid neurotransmission in fimbria-fornix fibers innervating the lateral septal complex of rats. Expl Brain Res. 54:1984;455-462.
22. Kermer P., Naumann T., Bender R., Frotscher M. Fate of GABAergic septohippocampal neurons after fimbria-fornix transection as revealed by in situ hybridization for glutamate decarboxylase mRNA and parvalbumin immunocytochemistry. J. comp. Neurol. 362:1995;385-399.
23. Köhler C., Chan-Palay V., Wu J.-Y. Septal neurons containing glutamic acid decarboxylase immunoreactivity project to the hippocampal region in the rat brain. Anat. Embryol. 169:1984;41-44.
24. Kromer L. F. Nerve growth factor treatment after brain injury prevents neuronal death. Science. 235:1987;214-216.
25. Leranth C., Frotscher M. Organization of the septal region in the rat brain: cholinergic-GABAergic interconnections and the termination of hippocampo-septal fibers. J. comp. Neurol. 289:1989;304-314.
26. Leranth C., Deller T., Buzsáki G. Intraseptal connections redefined: lack of a lateral septum to medial septum path. Brain Res. 583:1992;1-11.
27. Lieberman A. R. The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int. Rev. Neurobiol. 14:1971;49-124.
28. MacLean P. D. Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). Electroencephalogr. clin. Neurophysiol. 4:1952;407-418.
29. 3H]aspartate from the dorsolateral septum after electrical stimulation of the fimbria in vitro. Neuroscience. 5:1980;127-133.
30. Martin L. J., Blackstone C. D., Levey A. I., Huganir R. L., Price D. L. Cellular localizations of AMPA glutamate receptors within the basal forebrain magnocellular complex of rat and monkey. J. Neurosci. 13:1993;2249-2263.
31. Martin L. J., Blackstone C. D., Levey A. I., Huganir R. L., Price D. L. AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience. 53:1993;327-358.
32. Michel P. P., Agid Y. Death of septal cholinergic neurons produced by chronic exposure to glutamate is prevented by the noncompetitive NMDA receptor/channel antagonist, MK-801: role of nerve growth factor and nitric oxide. J. Neurosci. Res. 40:1995;764-775.
33. Milner T. A., Amaral D. G. Evidence for a ventral septal projection to the hippocampal formation of the rat. Expl Brain Res. 55:1984;579-585.
34. Naumann T., Kermer P., Frotscher M. Fine structure of rat septohippocampal neurons. III. Recovery of choline acetyltransferase immunoreactivity after fimbria-fornix transection. J. comp. Neurol. 350:1994;161-170.
35. Naumann T., Linke R., Frotscher M. Fine structure of rat septohippocampal neurons. I. Identification of septohippocampal projections neurons by retrograde tracing combined with electron microscopic immunocytochemistry and intracellular staining. J. comp. Neurol. 325:1992;207-218.
36. Naumann T., Peterson G. M., Frotscher M. Fine structure of rat septohippocampal neurons. II. A time course analysis following axotomy. J. comp. Neurol. 325:1992;219-242.
37. Nauta W. J. H. An experimental study of the fornix system in the rat. J. comp. Neurol. 104:1956;247-272.
38. Olney J. W. Glutamate-induced neuronal necrosis in the infant mouse hypothalamus. J. Neuropathol. exp. Neurol. 30:1971;75-90.
39. Olney J. W., Rhee V., Ho O. L. Kainic acid: a powerful neurotoxic analogue of glutamate. Brain Res. 77:1974;507-512.
40. Parnavelas J. G., Lynch G., Brecha N., Cotman C. W., Globus A. Spine loss and regrowth in hippocampus following deafferentation. Nature. 248:1974;71-73.
41. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates., 2nd edn. Academic, Sydney.
42. Peters A., Palay S. L. and Webster H. DeF. (1991) The Fine Structure of the Nervous System. Neurons and Their Supporting Cells., 3rd edn, p. 494. Oxford University Press, New York.
43. Peterson G. M., Naumann T., Frotscher M. Identified septohippocampal neurons survive axotomy: a fine-structural analysis in the rat. Neurosci. Lett. 138:1992;81-85.
44. Peterson G. M. A quantitative analysis of the crossed septohippocampal projection in the rat brain. Anat. Embryol. 180:1989;421-425.
45. Peterson G. M., Williams L. R., Varon S., Gage F. H. Loss of GABAergic neurons in medial septum after fimbria-fornix transection. Neurosci. Lett. 76:1987;140-144.
46. Petralia R. S., Wenthold R. J. Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. comp. Neurol. 318:1992;329-354.
47. Petralia R. S., Yokotani N., Wenthold R. J. Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J. Neurosci. 14:1994;667-696.
48. Phelan K. D., Hasuo H., Twery M. J., Gallagher J. P. Projection neurons in the rat dorsolateral septal nucleus possess recurrent axon collaterals. Neurosci. Lett. 97:1989;259-265.
49. Portera-Cailliau C., Price D. L., Martin L. J. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J. comp. Neurol. 378:1997;70-87.
50. Portera-Cailliau C., Price D. L., Martin L. J. Non-NMDA and NMDA receptor-mediated excitotoxic neuronal deaths in adult brain are morphologically distinct: further evidence for an apoptosis-necrosis continuum. J. comp. Neurol. 378:1997;88-104.
51. Raisman G. The connections of the septum. Brain. 89:1966;317-348.
52. Raisman G. A comparison of the mode of termination of the hippocampal and hypothalamic afferents to the septal nuclei as revealed by electron microscopy of degeneration. Expl Brain Res. 7:1969;317-343.
53. Raisman G. Neuronal plasticity in the septal nuclei of the adult rat. Brain Res. 14:1969;25-48.
54. Raisman G., Field P. M. A quantitative investigation of the development of collateral reinnervation after partial deafferentation of the septal nuclei. Brain Res. 50:1973;241-264.
55. Ramnath R. R., Strange K., Rosenberg P. A. Neuronal injury evoked by depolarizing agents in rat cortical cultures. Neuroscience. 51:1992;931-939.
56. Schramm M., Eimerl S., Costa E. Serum and depolarizing agents cause acute neurotoxicity in cultured cerebellar granule cells: role of the glutamate receptor responsive to N-methyl-D-aspartate. Proc. natn. Acad. Sci. U.S.A. 87:1990;1193-1197.
57. Sofroniew M. V., Galletly N. P., Isacson O., Svendsen C. N. Survival of adult basal forebrain cholinergic neurons after loss of target neurons. Science. 247:1990;338-342.
58. Storm-Mathisen J., Opsahl M. W. Aspartate and/or glutamate may be transmitters in hippocampal efferents to septum and hypothalamus. Neurosci. Lett. 9:1978;65-70.
59. Streit W. J. Microglial-neuronal interactions. J. Chem. Neuroanat. 6:1993;261-266.
60. Swanson L. W., Cowan W. M. Hippocampo-hypothalamic connections: origin in subicular cortex, not Ammon's horn. Science. 189:1975;303-304.
61. Swanson L. W., Cowan W. M. An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J. comp. Neurol. 172:1977;49-84.
62. Swanson L. W., Cowan W. M. The connections of the septal region in the rat. J. comp. Neurol. 186:1979;621-656.
63. Takahashi M., Liou S.-Y., Kunihara M. Ca2+- and Cl-dependent, NMDA receptor-mediated neuronal death induced by depolarization in rat hippocampal organotypic cultures. Brain Res. 675:1995;249-256.
64. Walaas I., Fonnum F. Biochemical evidence for glutamate as a transmitter in hippocampal efferents to the basal forebrain and hypothalamus in the rat brain. Neuroscience. 5:1980;1691-1698.
65. Wilcox B. J., Applegate M. D., Portera-Cailliau C., Koliatsos V. E. Nerve growth factor prevents apoptotic cell death in injured central cholinergic neurons. J. comp. Neurol. 359:1995;573-585.
66. Williams L. R., Varon S., Peterson G. M., Wictorin K., Fischer W., Björklund A., Gage F. H. Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix transection. Proc. natn. Acad. Sci. U.S.A. 83:1986;9231-9235.