Correlated axonal sprouting and dendritic spine formation during kainate-induced neuronal morphogenesis in the dentate gyrus of adult mice

Experimental Neurology

Volumn 145, Issue 1, 1997, Pages 203-213

  Suzuki, Fumio ^b   Makiura, Yaeko ^a   Guilhem, Didier ^a   Sørensen, Jens Christian ^c   Onteniente, Brigitte ^a  

^a Inst Nat Sante et de la Rech Med   (France)

^b SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

KAINIC ACID;

ANIMAL CELL; ARTICLE; DENDRITE; DENTATE GYRUS; ENTORHINAL CORTEX; GROWTH REGULATION; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL;

EID: 0031149604     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1997.6469     Document Type: Article

References (50)

1. Amaral D. G., Dent J. A. Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J. Comp. Neurol. 195:1981;51-86.
2. Andersen P., Trommald M. Possible strategies for finding the substrate for learning-induced changes in the hippocampal cortex. J. Neurobiol. 26:1995;396-402.
3. Bannister N. J., Larkman A. U. Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus. 2. Spine distributions. J. Comp. Neurol. 360:1995;161-171.
4. Ben-Ari Y., Represa A. Brief seizure episodes indicate long-term potentiation and mossy fiber sprouting in the hippocampus. Trends Neurosci. 13:1990;312-317.
5. Berger T. W., Semple-Rowland S., Basset J. L. Hippocampal polymorph neurons are the cells of origin for ipsilateral association and commissural afferents to the dentate gyrus. Brain Res. 215:1980;329-336.
6. Blackstad T. W., Kjaerheim A. Special axo-dendritic synapses in the hippocampal cortex: Electron and light microscopic studies on the layer of mossy fibers. J. Comp. Neurol. 117:1961;133-157.
7. Bliss T. V. P., Collingridge G. L. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature. 361:1993;31-39.
8. Calverley R. K. S., Jones D. G. Contributions of dendritic spines and perforated synapses to synaptic plasticity. Brain Res. 15:1996;215-249.
9. Cotman C. W. Specificity of synaptic growth in brain: Remodeling induced by kainic acid. Brain Res. 51:1979;203-215.
10. Davenport C. J., Brown W. J., Babb T. L. Sprouting of GABAergic and mossy fibers axons in the dentate gyrus following intrahippocampal kainate in the rat. Exp. Neurol. 109:1990;180-190.
11. Desmond N. L., Levy W. B. Granule cell dendritic spine density in the rat hippocampus varies with spine shape and location. Neurosci. Lett. 54:1985;219-224.
12. Fletcher T. L., De Camilli P., Banker G. Synaptogenesis in hippocampal cultures: evidence indicating that axons and dendrites become competent to form synapses at different stages of neuronal development. J. Neurosci. 14:1994;6695-6706.
13. Frotscher M., Zimmer J. Lesion-induced mossy fibers sprouting to the molecular layer of the rat fascia dentata: Identification of post-synaptic granule cells by the Golgi-EM technique. J. Comp. Neurol. 215:1983;299-311.
14. Frotscher M., Lérànth C. The cholinergic innervation of the rat fascia dentata: Identification of target structures on granule cells by combining choline acetyltransferase immunocytochemistry and Golgi impregnation. J. Comp. Neurol. 243:1986;53-70.
15. Frotscher M., Hàmori J., Wenzel J. Transneuronal effects of entorhinal lesions in the early postnatal period on synaptogenesis in the hippocampus of the rat. Brain Res. 30:1977;549-560.
16. Frotscher M., Deller T., Heimrich B., Förster E., Haas C., Naumann T. Survival, regeneration and sprouting of central neurons: The rat septo-hippocampal projection as a model. Ann. Anat. 178:1996;311-315.
17. Gaiarsa J. L., Beaudoin M., Ben-Ari Y. Effect of neonatal degranulation on the morphological development of rat CA3 pyramidal neurons: Inductive role of mossy fibers on the formation of thorny excrescences. J. Comp. Neurol. 321:1992;612-625.
18. Geinisman Y., Detoledomorrell L., Morrell F. Induction of long-term potentiation is associated with an increase in the number of axospinous synapses with segmented postsynaptic densities. Brain Res. 566:1991;77-88.
19. Goodman J. H., Sloviter R. S. Evidence for commissurally projecting parvalbumin-immunoreactive neurons in the dentate gyrus of the rat. Hippocampus. 2:1992;13-22.
20. Guilhem D., Dreyfus P., Makiura Y., Suzuki F., Onteniente B. Short increase of BDNF messenger RNA triggers kainic acid-induced neuronal hypertrophy in adult mice. Neuroscience. 72:1996;923-931.
21. Gulyas A. I., Miettinen R., Jacobowitz D. M., Freund T. F. Calretinin is present in non-pyramidal cells of the rat hippocampus-I. A new type of neuron specifically associated with the mossy fiber system. Neuroscience. 48:1992;1-27.
22. Harris K. M., Kater S. B. Dendritic spines: Cellular specializations imparting both stability and flexibility to synaptic function. Annu. Rev. Neurosci. 17:1994;341-371.
23. Haug F. M. S. Heavy metals in the brain. A light microscopy study of the rat with Timm's sulfide silver method. Methodological considerations and cytological and regional staining patterns. Ergebn Anat. Entwickl-Gesch. 47:1973;1-71.
24. Hauser C. R. Morphological changes in the dentate gyrus in human temporal lobe epilepsy. The Dentate Gyrus and Its Role in Seizures. 1992;Elsevier, Amsterdam. p. 223-234.
25. Heimrich B., Papp EC., Freund TF., Frotscher M. Regeneration of the gabaergic septohippocampal projection in vitro. Neuroscience. 72:1996;409-417.
26. Hosokawa T., Bliss TVP., Fine A. Persistence of individual dendritic spines in living brain slices. Neuroreport. 3:1992;477-480.
27. Liu Y., Fujise N., Kosaka T. Distribution of calretinin immunoreactivity in the mouse dentate gyrus. I. General description. Exp. Brain Res. 108:1996;389-403.
28. Laurberg S., Sorensen KE. Associational and commissural collaterals of neurons in the hippocampal formation (hilus fasciae dentatae and subfield CA3). Brain Res. 212:1981;433-459.
29. Laurberg S., Zimmer J. Lesion-induced sprouting of hippocampal mossy fiber collaterals to the fascia dentata in developing and adult rats. J. Comp. Neurol. 200:1981;433-459.
30. Lynch G., Stanfield B., Parks T., Cotman CW. Evidence for selective post lesion axonal growth in dentate gyrus of the rat. Brain Res. 69:1974;1-11.
31. Magloczky Z. S., Freund T. F. Selective neuronal death in the contralateral hippocampus following unilateral kainate injections into the CA3 subfield. Neuroscience. 56:1993;317-336.
32. Matthews DA., Cotman C., Lynch G. An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of adult rat. I. Magnitude and time course of degeneration. Brain Res. 115:1976;1-21.
33. Moser M. B., Trommald M., Andersen P. An increase in dentritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc. Natl. Acad. Sci. USA. 91:1994;12673-12675.
34. Nadler J. V., Perry B. W., Cottman 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.
35. Nitsch R., Leranth C. Calretinin immunoreactivity in the monkey hippocampal formation-II. Intrinsic GABAergic and hypothalamic non-GABAergic systems: An experimental tracing and co-existence study. Neuroscience. 55:1993;797-812.
36. Nitsch R., Ohm T. G. Calretinin immunoreactive structures in the human hippocampal formation. J. Comp. Neurol. 360:1995;475-487.
37. Papa M., Segal M. Morphological plasticity in dendritic spines of cultured hippocampal neurons. Neuroscience. 71:1996;1005-1011.
38. Parnavelas J. G., Lynch G., Brecha H., Cottman C. W., Globus A. Spine loss and regrowth in hippocampus following deafferentation. Nature. 248:1974;71-73.
39. Patton P. E., McNaughton B. Connection matrix of the hippocampal formation. 1. The dentate gyrus. Hippocampus. 5:1995;245-286.
40. Represa A., Ben-Ari Y. Kindling is associated with the formation of novel mossy fiber synapses in the CA3 region. Brain Res. 92:1992;69-78.
41. Schauwecker P. E., McNeill T. H. Enhanced but delayed axonal sprouting of the commissural/associational pathway following a combined entorhinal cortex/fimbria fornix lesion. J. Comp. Neurol. 351:1995;453-464.
42. Sorensen J. C., Tonder N., Zimmer J. Biocytin Pellets - An alternative technique for massive anterograde labeling of neuronal pathways in vivo and in vitro. Brain Res. 608:1993;338-344.
43. Sutula T., Xian-Xian H., Cavazos J., Scott G. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science. 239:1988;1147-1150.
44. Suzuki F., Junier M. P., Guilhem D., Sorensen J. C., Onteniente B. Morphogenetic effect of kainate on adult hippocampal neurons associated with a prolonged expression of brain-derived neurotrophic factor. Neuroscience. 64:1995;665-674.
45. Tago H., Kimura H., Maeda T. Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. J. Histochem. Cytochem. 34:1986;1431-1438.
46. Tauck D., Nadler J. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 5:1985;1016-1022.
47. Trommald M., Line Vaaland J., Blackstad T. W., Andersen P. Dendritic spine changes in rat dentate granule cells associated with long-term potentiation. Guidotti A. Neurotoxicity of Excitatory Amino Acids. 1990;163-174 Raven Press, New York.
48. West Jr., Dewey S. L. Mossy fiber sprouting in the fascia dentata after unilateral entorhinal lesions: Quantitative analysis using computer-assisted image processing. Neuroscience. 13:1984;377-384.
49. Zafirov S., Heimrich B., Frotscher M. Dendritic development of dentate granule cells in the absence of their specific extrinsic afferents. J. Comp. Neurol. 345:1994;472-480.
50. Zimmer J. Extended commissural and ipsilateral projections in postnatally deentorhinated hippocampus and fascia dentata demonstrated in rats by silver impregnation. Brain Res. 64:1973;293-311.