Delayed death of septal cholinergic neurons after excitotoxic ablation of hippocampal neurons during early postnatal development in the rat

Experimental Neurology

Volumn 139, Issue 1, 1996, Pages 143-155

  Cooper, Jonathan D ^a,b   Skepper, Jeremy N ^a   Berzaghi, Maria Da Penha ^b   Lindholm, Dan ^b   Sofroniew, Michael V ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EXCITOTOXIN; N METHYL DEXTRO ASPARTIC ACID; NERVE GROWTH FACTOR;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN INJURY; CELL DEATH; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MORPHOMETRICS; NONHUMAN; PRIORITY JOURNAL; RAT; ULTRASTRUCTURE;

EID: 0029994286     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1996.0089     Document Type: Article

References (60)

1. ABERCROMBIE, M. 1946. Estimation of nuclear populations from microtome sections. Anat. Rec. 94: 239-247.
2. ALDERSON, R. F., A. L. ALTERMAN, Y-A. BARDE, AND R. M. LINDSAY. 1990. Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture. Neuron 5: 297-306.
3. ARENDT, T., M. K. BRÜCKNER, T. KRELL, S. PAGLIUSI, L. KRUSKA, AND R. HEUMANN. 1995. Degeneration of rat cholinergic basal forebrain neurons and reactive changes in nerve growth factor expression after chronic neurotoxic injury II. Reactive expression of the nerve growth factor gene in astrocytes. Neuroscience 65: 647-659.
4. ARMSTRONG, D. M., G. BRUCE, L. B. HERSH, AND F. H. GAGE. 1987. Development of cholinergic neurons in the septal/diagonal band complex of the rat. Dev. Brain Res. 36: 249-256.
5. AUBURGER, G., R. HEUMANN, R. HELLWEG, S. KORSCHING, AND H. THOENEN. 1987. Developmental changes of nerve growth factor and its mRNA in the rat hippocampus: comparison with choline acetyltransferase. Developmental Biol. 120: 322-328.
6. 3H-thymidine autoradiography. J. Comp. Neurol. 183: 89-106.
7. BAYER, S. A., AND J. ALTMAN. 1974. Hippocampal development in the rat: Cytogenesis and morphogenesis examined with autoradiography and low-level x-irradiation. J. Comp. Neurol. 158: 55-80.
8. BURKE, M. A., J. R. APTER, B. H. WAINER, E. J. MUFSONAND, AND J. H. KORDOWER. 1994. Age-related vulnerability of developing cholinergic basal forebrain neurons following excitotoxic lesions of the hippocampus. Exp. Neurol. 128: 159-171.
9. BURKE, M. A., W. C. MOBLEY, J. CHO, S. J. WIEGAND, R. M. LINDSAY, E. J. MUFSON, AND J. H. KORDOWER. 1994. Loss of developing cholinergic basal forebrain neurons following excitotoxic lesions of the hippocampus: Rescue by neurotrophins. Exp. Neurol. 130: 178-195.
10. CHANDLER, C. E., L. M. PARSONS, M. HOSANG, AND E. SHOOTER. 1984. A monoclonal antibody modulates the interaction of nerve growth factor with PC12. J. Biol. Chem. 259: 6882-6889.
11. CHEN, K. S., M. C. NISHIMURA, S. SPENCER, C. CROWLEY, AND H. S. PHILLIPS. 1994. Learning, memory and the basal forebrain cholinergic system in aged mice heterozygous for nerve growth factor deletion. Soc. Neurosci. Abstr. 20: 856.
12. CHOMCZYNSKI, P., AND N. SACCHI. 1987. Single-step method of RNA isolation by acid guanidium-thiocynate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159.
13. CLARKE, P. G. H. 1990. Developmental cell death: Morphological diversity and multiple mechanisms. Anat. Embryol. 181: 195-213.
14. COWAN, W. N., J. W. FAWCETT, D. M. O'LEARY, AND B. B. STANFIELD. 1984. Regressive events in neurogenesis. Science 225: 1258-1264.
15. COYLE, J. T., AND R. SCHWARTZ. 1983. The use of excitatory amino acids as selective neurotoxins. In Handbook of Chemical Neuroanatomy, Vol. 1, Methods in Chemical Neuroanatomy (A. Björklund and T. Hökfelt, Eds.), pp. 508-527. Elsevier, Amsterdam.
16. CRAIN, B., C. COTMAN, D. TAYLOR, AND G. LYNCH. 1973. A quantitative electron microscopic study of synaptogenesis in the dentate gyrus of the rat. Brain Res. 63: 195-204.
17. CROWLEY, C., S. D. SPENCER, M. C. NISHIMURA, K. S. CHEN, S. PITTS-MEEK, M. P. ARMANINI, L. H. LING, S. B. MCMAHON, D. L. SHETTON, A. D. LEVINSON, AND H. S. PHILLIPS. 1994. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76: 1001-1011.
18. CRUTCHER, K. A. 1982. Development of the rat septohippocampal projection: Aretrograde fluorescent tracer study. Dev. Brain Res. 3: 145-150.
19. CUELLO, A. C., AND M. V. SOFRONIEW. 1984. The anatomy of the CNS cholinergic neurons. Trends Neurosci. 7: 74-78.
20. ECKENSTEIN, F., AND H. THEONEN. 1982. Production of specific antisera and monoclonal antibodies to choline acetyltransferase; characterization and use for identification of cholinergic neurons. EMBO J. 1: 363-368.
21. EICHLER, M. E., AND K. M. RICH. 1989. Death of sensory ganglion neurons after acute withdrawal of nerve growth factor in dissociated cell cultures. Brain Res. 482: 340-346.
22. GAGE, F. H., P. BATCHELOR, K. S. CHEN, D. CHIN, G. A. HIGGINS, S. KOH, S. DEPUTY, M. B. ROSENBERG, W. FISCHER, AND A. BJORKLUND. 1989. NGF receptor reexpression and NGF-mediated cholinergic neuronal hypertrophy in the damaged adult neostriatum. Neuron 2: 1177-1184.
23. GASSER, U. E., G. WESKAMP, U. OTTEN, AND A. R. DRAVID. 1986. Time course of the elevation of nerve growth factor (NGF) contents in the hippocampus and septum following lesions of the septo-hippocampal pathway in rats. Brain Res. 376: 351-356.
24. GNAHN, H., F. HEFTI, R. HEUMANN, M. E. SCHWAB, AND H. THOENEN. 1983. NGF-mediated increase of choline acetyltransferase (ChAT) in the neonatal rat forebrain: Evidence for a physiological role of NGF in the brain. Dev. Brain Res. 9: 45-52.
25. GRIMES, M., J. ZHOU, Y. LI, D. HOLTZMAN, AND W. C. MOBLEY. 1993. Neurotrophin signalling in the nervous system. Semin. Neurosci. 5: 239-247.
26. HARTIKKA, J., AND F. HEFTI. 1988. Development of septal cholinergic neurons in culture: Plating density and glial cells modulate effects of NGF on survival, fibre growth, and expression of transmitter-specific enzymes. J. Neurosci. 8: 2967-2985.
27. HEFTI, F. 1986. Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J. Neurosci. 6: 2155-2162.
28. HIGGINS, G. A., S. KOH, K. S. CHEN, AND F. H. GAGE. 1989. NGF induction of NGF receptor gene expression and cholinergic neuronal hypertrophy within the basal forebrain of the adult rat. Neuron 3: 247-256.
29. ISACSON, O., AND M. V. SOFRONIEW. 1992. Effects of neuronal loss and replacement in the cerebral cortex on intrinsic and afferent neuronal systems: neurochemical and morphologic evidence for plasticity in the injured adult neocortex. Exp. Neurol. 117: 151-175.
30. JONES, K. W., I. FARINAS, C. BACKUS, AND L. F. REICHARDT. 1994. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76: 989-999.
31. KAWAJA, M. D., AND F. H. GAGE. 1991. Nerve growth factor receptor immunoreactivity in the rat septohippocampal pathway: A light and electron microscope investigation. J. Comp. Neurol. 307: 517-529.
32. +. Neuroscience 72: in press.
33. KOH, S., AND R. LOY.1989. Localization and development of nerve growth factor-sensitive rat basal forebrain neurons and their afferent projections to hippocampus and neocortex. J. Neurosci. 9: 2999-3018.
34. KORDOWER, J. H., M. BURKE-WATSON, J. D. ROBACK, AND B. H. WAINER. 1993. Stability of septohippocampal neurons following excitotoxic lesions of the rat hippocampus. Exp. Neurol. 117: 1-16.
35. LAMS, B. E., ISACSON, O., AND SOFRONIEW, M. V. 1988. Loss of transmitter-associated enzyme staining following axotomy does not indicate death of brainstem cholinergic neurons. Brain Res. 475: 401-406.
36. LEVI-MONTALCINI, R., AND P. ANGELETTI. 1968. Nerve growth factor. Physiol. Rev. 48: 534-569.
37. LINDHOLM, D., R. HEUMANN, M. MEYER, AND H. THOENEN. 1987. Interleukin-1 regulates synthesis of nerve growth factor in non-neuronal cells of rat sciatic nerve. Nature 330: 658-659.
38. NAUMANN, T., G. M. PETERSON, AND M. FROTSCHER. 1992. Fine structure of rat septohippocampal neurons. I. Identification of septohippocampal projection neurons by retrograde tracing combined with electron microscopic immunohistochemistry and intracellular staining. J. Comp. Neurol. 325: 219-242.
39. O'BRIEN, T. S., C. N. SVENDSEN, O. ISACSON, AND M. V. SOFRONIEW. 1990. Loss of True blue labelling from the medial septum following transection of the fimbria-fornix: Evidence for the death of cholinergic and noncholinergic neurons. Brain Res. 508: 249-256.
40. OPPENHEIM, R. W. 1989. The neurotrophic theory and naturally occuring motoneuron cell death. Trends Neurosci. 12: 252-255.
41. PERSSON, H. 1993. Neurotrophin production in the brain. Semin. Neurosci. 5: 227-237.
42. PLASCHKE, M., E. M. KASPER, T. NAUMANN, AND M. FROTSCHER. 1994. Survival and transmitter expression of rat cholinergic medial septal neurons despite removal of hippocampus in the early post natal period. Neurosci. Lett. 176: 243-246.
43. SAPORITO, M. S., AND S. CARSWELL. 1995. High levels and local effects of nerve growth factor in the septal region of the adult rat brain. J. Neurosci. 15: 2280-2286.
44. SEILER, M., AND M. SCHWAB. 1984. Specific retrograde transport of nerve growth factor (NGF) from neocortex to nucleus basalis in the rat. Brain Res. 300: 33-39.
45. SEMBA, K., AND H. C. FIBIGER. 1988. Time of origin of cholinergic neurons in the rat basal forebrain. J. Comp. Neurol. 269: 87-95.
46. SHELTON, D. L., J. V. NADLER, AND C. W. COTMAN. 1979. Development of high affinity choline uptake and associated acetylcholine synthesis in the rat fascia dentata. Brain Res. 163: 263-275.
47. SMEYNE, R. J., R. KLEIN, A. SCHNAPP, L. K. LONG, S. BRYANT, A. LEWIN, S. A. LIRA, AND M. BARBACID. 1994. Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/ NGF receptor gene. Nature 368: 246-249.
48. SOFRONIEW, M. V., AND O. ISACSON. 1988. Distribution of degeneration of cholinergic neurons in the septum following axotomy in different portions of the fimbria-fornix: A correlation between degree of cell loss and proximity of neuronal somata to the lesion. J. Chem. Neuroanat. 1: 327-337.
49. SOFRONIEW, M. V., J. D. COOPER, C. N. SVENDSEN, P. CROSSMAN, N. Y. IP, R. M. LINDSAY, F. ZAFRA, AND D. LINDHOLM. 1993. Atrophy but not death of adult septal cholinergic neurons after ablation of target capacity to produce mRNAs for NGF, BDNF, and NT3. J. Neurosci. 13: 5263-5276.
50. SOFRONIEW, M. V., N. P. GALLETLY, O. ISACSON, AND C. N. SVENDSEN. 1990. Survival of adult basal forebrain cholinergic neurons after loss of target neurons. Science 247: 338-342.
51. SOFRONIEW, M. V., R. C. A. PEARSON, AND T. P. S. POWELL. 1987. The cholinergic nuclei of the basal forebrain of the rat: Normal structure, development and experimentally induced degeneration. Brain Res. 411: 310-331.
52. SOFRONIEW, M. V., AND J. D. COOPER. 1993. Neurotrophic mechanisms and neuronal degeneration. Semin. Neurosci. 5: 285-294.
53. SPRANGER, M., D. LINDHOLM, C. BANDTLOW, R. HEUMANN, H. GNAHN, M. NAHER-NOE, AND H. THOENEN. 1990. Regulation of nerve growth factor (NGF) synthesis in the rat central nervous system: Comparison between the effects of interleukin-1 and various growth factors in astrocyte cultures and in vivo. Eur. J. Neurosci. 2: 69-76.
54. SVENDSEN, C. N., J. N. C. KEW, K. STALEY, AND M. V. SOFRONIEW. 1994. NGF withdrawal results in the death of developing but not mature septal cholinergic neurons in vitro: Protection by protein synthesis inhibition. J. Neurosci. 14: 75-87.
55. TUSZYNSKI, M. H., D. M. ARMSTRONG, AND F. H. GAGE. 1990. Basal forebrain cell loss following fimbria/fornix transection. Brain Res. 508: 241-248.
56. VANTINI, G., N. SCHIAVO, A. DI MARTINO, P. POLATO, C. TRIBAN, L. CALLEGARO, G. TOFFANO, AND A. LEON. 1989. Evidence for a physiological role of nerve growth factor in the central nervous system of neonatal rats. Neuron 3: 267-273.
57. WIDMER, H. R., B. KNÜSSEL, AND F. HEFTI. 1993. BDNF protection of basal forebrain cholinergic neurons after axotomy: complete protection of p75NGFR-positive cells. Neuroreport 4: 363-366.
58. WILLIAMS, L. R., S. VARON, G. M. PETERSON, K. WICTORIN, W. FISCHER, A. BJORKLUND, AND F. H. GAGE. 1986. Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix trasection. Proc. Natl. Acad. Sci. USA 83: 9231-9235.
59. WOOD, S. J., J. PRITCHARD, AND M. V. SOFRONIEW. 1990. Reexpression of nerve growth factor receptor after axonal injury recapitulates a developmental event in motor neurons: Differential regulation when regeneration is allowed or prevented. Eur. J. Neurosci. 2: 650-658.
60. ZAFRA, F., B. HENGERER, J. LEIBROCK, H. THOENEN, AND D. LINDHOLM. 1990. Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J. 9: 3545-3550.