The process of reinnervation in the dentate gyrus of adult rats: Physiological events at the time of the lesion and during the early postlesion period

Experimental Neurology

Volumn 139, Issue 1, 1996, Pages 73-82

  Kelley, Melinda S ^a   Steward, Oswald ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; DENTATE GYRUS; ELECTROENCEPHALOGRAM; ELECTROPHYSIOLOGY; ENTORHINAL CORTEX; EVOKED RESPONSE; MALE; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SEIZURE;

EID: 0029975635     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1996.0082     Document Type: Article

References (54)

1. BAUDRY, M., G. LYNCH, AND C. GALL. 1986. Induction of ornithine decarboxylase as a possible mediator of seizure-induced changes in genomic expression in rat hippocampus. J. Neurosci. 6: 3430-3435.
2. BENOWITZ, L. I., W. R. RODRIGUEZ, AND R. L. NEVE. 1990. The pattern of GAP-43 immunostaining changes in the rat hippocampal formation during reactive synaptogenesis. Mol. Brain Res. 8: 17-23.
3. BONTHIUS, D. J., AND O. STEWARD. 1993. Induction of cortical spreading depression with potassium chloride upregulates levels of messenger RNA for glial fibrillary acidic protein in cortex and hippocampus: Inhibition by MK-801. Brain Res. 618: 83-94.
4. BUSCIGLIO, J., A. FERREIRA, O. STEWARD, AND A. CACERES. 1987. An immunocytochemical and biochemical study of the microtubule associated protein Tau during post-lesion afferent reorganization in the hippocampus of adult rats. Brain Res. 419: 244-252.
5. CACERES, A., J. BUSCIGLIO, A. FERREIRA, AND O. STEWARD. 1988. An immunocytochemical and biochemical study of the microtubule associated protein MAP-2 during post-lesion dendritic remodeling in the central nervous system of adult rats. Brain Res. 427: 233-246.
6. CAMPBELL, K. A., B. BANK, AND N. W. MILGRAM. 1984. Epileptogenic effects of electrolytic lesions in the hippocampus: role of iron deposition. Exp. Neurol. 86: 506-514.
7. CONNER, J. M., B. FASS-HOLMES, AND S. VARON. 1994. Changes in nerve growth factor immunoreactivity following entorhinal cortex lesions: Possible molecular mechanism regulating cholinergic sprouting. J. Comp. Neurol. 345: 409-418.
8. COTMAN, C. W., AND J. V. NADLER. 1978. Reactive synaptogenesis in the hippocampus. In Neuronal Plasticity (C. Cotman, Ed.), pp. 227-271. Raven Press, New York.
9. DASHEIFF, R. M., AND J. O. MCNAMARA. 1982. Electrolytic entorhinal lesions cause seizures. Brain Res. 231: 444-450.
10. DELGADO, J., AND M. SEVILLANO. 1961. Evolution of repeated hippocampal seizures in the cat. Electroeceph. Clin. Neurophysiol. 13: 722-733.
11. FAGAN, A. M., AND F. H. GAGE. 1990. Cholinergic sprouting in the hippocampus: A proposed role for IL-1. Exp. Neurol. 110: 105-120.
12. GALL, C. M., AND P. J. ISACKSON. 1989. Limbic seizures increase neuronal production of messenger RNA for nerve-growth factor. Science 245: 758-761.
13. GALL, C. M., R. BERSCHAUER, AND P. J. ISACKSON. 1994. Seizures increase basic fibroblast growth factor mRNA in adult rat forebrain neurons and glia. Mol. Brain Res. 21: 190-205.
14. GEDDES, J. W., E. J. HESS, R. A. HART, J. P. KESSLAK, C. W. COTMAN, AND M. C. WILSON. 1990. Lesions of hippocampal circuitry define synaptosomal-associated protein-25 (SNAP-25) as a novel presynaptic marker. Neuroscience 38: 515-525.
15. GEDDES, J. W., M. C. WILSON, F. D. MILLER, AND C. W. COTMAN. 1990. Molecular markers of reactive plasticity. Adv. Exp. Med. Biol. 268: 425-432.
16. GODDARD, G. 1967. Development of epileptic seizures through brain stimulation at low intensity. Nature 214: 1020-1021.
17. GOMEZ-PINILLA, F., J. W.-K. LEE, AND C. W. COTMAN. 1992. Basic FGF in adult rat brain: Cellular distribution and response to entorhinal lesion and fimbria-fornix transection. J. Neurosci. 12: 345-355.
18. GUTHRIE, K. M., T. NGUYEN, AND C. M. GALL. 1995. Insulin-like growth factor-1 mRNA is increased in deafferented hippocampus: Spatiotemporal correlation of a trophic event with axon sprouting. J. Comp. Neurol. 352: 147-160.
19. GWAG, B. J., F. SESSLER, K. KIMMERER, AND J. E. SPRINGER. 1994. Neurotrophic factor mRNA expression in dentate gyrus is increased following angular bundle transection. Brain Res. 647: 23-29.
20. HANSEN, A. J., AND T. ZEUTHEN. 1981. Extracellular ion concentrations during spreading depression and ischemia in the rat brain cortex. Acta Physiol. Scand. 113: 437-445.
21. HANSEN, A., O. S. JORGENSEN, T. G. BOLWIG, AND D. I. BARRY. 1991. Hippocampal kindling in the rat is associated with time-dependent increases in the concentration of glial fibrillary acidic protein. J. Neurochem. 57: 1716-1720.
22. HERDEGEN, T., J. SANDKUHLER, P. GASS, M. KIESSLING, R. BRAVO, AND M. ZIMMERMAN. 1993. JUN, FOS, KROX, and CREB transcription factor proteins in the rat cortex: Basal expression and induction by spreading depression and epileptic seizures. J. Comp. Neurol. 333: 271-288.
23. HERRERA, D. G., AND H. A. ROBERTSON. 1990. Application of potassium chloride to the brain surface induces the c-fos protooncogene: Reversal by MK-801. Brain Res. 510: 166-190.
24. HERRERA, D. G., D. MAYSINGER, R. GADIENT, C. BOECKH, U. OTTEN, AND A. C. CUELLO. 1993. Spreading depression induced c-fos-like immunoreactivity and NGF mRNA in the rat cerebral cortex. Brain Res. 602: 99-103.
25. ISACKSON, P. J., M. M. HUNTSMAN, K. D. MURRAY, AND C. M. GALL. 1991. BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: Temporal patterns of induction distinct from NGF. Neuron 6: 937-948.
26. KRAIG, R. P., AND C. NICHOLSON. 1978. Extracellular ionic variations during spreading depression. Neuroscience 3: 1045-1059.
27. KRAIG, R. P., L. DONG, R. THISTED, AND C. B. JAEGER. 1991. Spreading depression increases immunohistochemical staining of glial fibrillary acidic protein. J. Neurosci. 11: 2187-2198.
28. KREUTZBERG, G. W. 1995. Microglia, the first line of defence in brain pathologies. Arzneimittelforschung 45: 357-360.
29. KUBOTA, M., T. NAKAMURA, K. SUNAMI, Y. OZAWA, H. NAMBA, A. YAMAURA, AND H. MAKINO. 1989. Changes of local cerebral glucose utilization, DC potential and extracellular potassium concentration in experimental head injury of varying severity. Neurosurg. Rev. 12: 393-339.
30. KWAK, S., AND A. MATUS. 1988. Denervation induces long-lasting changes in the distribution of microtubule proteins in hippocampal neurons. J. Neurocytol. 17: 189-195.
31. LAPING, N. J., T. E. MORGAN, N. R. NICHOLS, I. ROZOVSKY, C. S. YOUNG-CHAN, C. ZAROW, AND C. E. FINCH. 1994. Transforming growth factor-beta 1 induced neuronal and astrocyte genes: Tubulin alpha 1, glial fibrillary acidic protein and clusterin. Neuroscience 58: 563-572.
32. LAUTERBORN, J. C., P. J. ISACKSON, AND C. M. GALL. 1994. Seizure-induced increases in NGF mRNA exhibit different time courses across forebrain regions and are biphasic in hippocampus. Exp. Neurol. 125: 22-40.
33. LEAO, A. A. P. 1944. Spreading depression of activity in the cerebral cortex. J. Neurophysiol. 7: 359-390.
34. LINDSAY, R. M. 1986. Reactive gliosis. In Astrocytes: Cell Biology and Pathology of Astrocytes (S. Fedoroff and A. Vernadakis, Eds.), pp. 231-262. Academic Press, Orlando.
35. LOESCHE, J., AND O. STEWARD. 1977. Behavioral correlates of denervation and reinnervation of the hippocampal formation of the rat: Recovery of alternation performance following unilateral entorhinal cortex lesions. Brain Res. Bull. 2: 31-39.
36. LOTHMAN, E. W., J. M. HATLELID, C. F. ZORUMSKI, J. A. CONRY, P. F. MOON, AND J. B. PERLIN. 1985. Kindling with rapidly recurring hippocampal seizures. Brain Res. 360: 83-91.
37. MATTHEWS, D. A., C. COTMAN, AND G. LYNCH. 1976. An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. I. Magnitude and time course of degeneration. Brain Res. 115: 1-21.
38. MATTHEWS, D. A., C. COTMAN, AND G. LYNCH. 1976. An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. II. Reappearance of morphologically normal synaptic contacts. Brain Res. 115: 23-41.
39. MORGAN, J. I., D. R. COHEN, J. L. HEMPSTEAD, AND T. CURRAN. 1987. Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237: 192-197.
40. NICHOLS, N. R., N. J. LAPING, J. R. DAY, AND C. E. FINCH. 1991. Increases in transforming growth factor-beta mRNA in hippocampus during response to entorhinal cortex lesions in intact and adrenalectomized rats. J. Neurosci. Res. 28: 134-139.
41. NIEDERMEYER, E. 1987. Abnormal EEG patterns (epileptic and paroxysmal). In Electroencephalography: Basic Principles, Clinical Applications, and Related Fields (E. Niedermeyer and F. Lopes da Silva, Eds.), pp. 183-207. Urban and Schwarzenberg, Baltimore.
42. RACINE, R. J. 1972. Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroenceph. clin. Neurophysiol. 32: 281-294.
43. RACINE, R. J., J. G. GARTNER, AND W. M. BURNHAM. 1972. Epileptiform activity and neural plasticity in limbic structures. Brain Res. 47: 262-268.
44. REID, K. H., R. MARRANNES, E. DE PRINS, AND A. WAUQUIER. 1987. Potassium translocation and spreading depression induced by electrical stimulation of the brain. Exp. Neurol. 97: 345-364.
45. SAFFEN, D. W., A. J. COLE, P. F. WORLEY, B. A. CHRISTY, K. RYDER, AND J. M. BARABAN. 1988. Convulsant-induced increase in transcription factor messenger RNAs in rat brain. Proc. Natl. Acad. Sci. USA 85: 7795-7799.
46. STEWARD, O. 1986. Lesion-induced synapse growth in the hippocampus: in search of cellular and molecular mechanisms. In The Hippocampus (R. L. Isaacson and K. H. Pribram, Eds.), Vol. 3, pp. 65-111. Plenum Publishing, New York.
47. STEWARD, O. 1994. Electroconvulsive seizures upregulate astroglial gene expression selectively in the dentate gyrus. Mol. Brain Res. 25: 217-224.
48. STEWARD, O. 1995. The process of reinnervation in the dentate gyras of adult rats: gene expression by neurons during the period of lesion-induced growth. J. Comp. Neurol. 359: 391-411.
49. STEWARD, O., AND S. V. VINSANT. 1983. The process of reinnervation in the dentate gyrus of the adult rat. A quantitative electron microscopic analysis of terminal proliferation and reactive synaptogenesis. J. Comp. Neurol. 214: 370-386.
50. STEWARD, O., E. R. TORRE, L. L. PHILLIPS, AND P. A. TRIMMER. 1990. The process of reinnervation in the dentate gyrus of adult rats: Time course of increases in mRNA for glial fibrillary acidic protein. J. Neurosci. 10: 2373-2384.
51. STEWARD, O., E. R. TORRE, R. TOMASULO, AND E. LOTHMAN. 1991. Neuronal activity up-regulates astroglial gene expression. Proc. Natl. Acad. Sci. USA 88: 6819-6823.
52. SUGAYA, E., M. TAKATO, AND Y. NODA. 1975. Neuronal and glial activity during spreading depression in the cerebral cortex of cat. J. Neurophysiol. 38: 841-882.
53. SUNAMI, K., T. NAKAMURA, M. KUBOTA, Y. OZAWA, H. NAMBA, A. YAMURA, AND H. MAKINO. 1989. Spreading depression following experimental head injury in the rat. Neurol. Med. Chir. 29: 975-980.
54. YABLON, S. A. 1993. Posttraumatic seizures. Arch. Phys. Med. Rehab. 74: 983-1001.