Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles

Journal of Comparative Neurology

Volumn 406, Issue 4, 1999, Pages 449-460

  Markakis, Eleni A ^a   Gage, Fred H ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Adult neurogenesis; Fluoro Gold; Granule cells; Hippocampus; Retrograde tracing; Synaptophysin

Indexed keywords

BROXURIDINE; CALBINDIN; FLUOROGOLD; SYNAPTOPHYSIN;

ADULTHOOD; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CELL LABELING; DENTATE GYRUS; GRANULE CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT; SENESCENCE; SYNAPSE VESICLE; TISSUE SECTION;

ANIMALS; AXONS; BROMODEOXYURIDINE; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; DENTATE GYRUS; FLUORESCENT DYES; IMMUNOHISTOCHEMISTRY; IONTOPHORESIS; MALE; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; STILBAMIDINES; SYNAPTIC VESICLES; SYNAPTOPHYSIN;

EID: 0033583580     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990419)406:4<449::AID-CNE3>3.0.CO;2-I     Document Type: Article

References (57)

1. Altman J, Bayer SA. 1990a. Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301:365-381.
2. Altman J, Bayer SA. 1990b. Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 301:325-342.
3. Altman J, Das GD. 1965. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124: 319-336.
4. Alvarez-Buylla A. 1990. Mechanism of neurogenesis in adult avian brain. Experientia 46:948-955.
5. Amaral DG. 1978. A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182:851-914.
6. Amaral DG, Witter MP. 1995. Hippocampal formation. In: G. Paxinos, editor The rat nervous system. San Diego: Academic Press. p 443-493.
7. Angevine JB. 1965. Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp Neurol 13:1-70.
8. Aubert I, Ridet J-L, Schachner M, Rougon G, Gage FH. 1998. Expression of L1 and PSA during sprouting and regeneration in the adult hippocampal formation. J Comp Neurol 399:1-19.
9. Bayer SA. 1982. Changes in the total number of dentate granule cells in juvenile and adult rats: a correlated volumetric and 3H-thymidine autoradiographic study. Exp Brain Res 46:315-323.
10. Bayer SA, Yackel JW, Puri PS. 1982. Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216:890-892.
11. Bernocchi G, Scherini E, Giacometti S, Mares V. 1990. Premitotic DNA synthesis in the brain of the adult frog (Rana esculenta L.): an autoradiographic 3H-thymidine study. Anat Rec 228:461-470.
12. Berod A, Hartman BK, Pujol JF. 1981. Importance of fixation in immunohistochemistry: use of formaldehyde solutions at variable pH for the localization of tyrosine hydroxylase. J Histochem Cytochem 29: 844-850.
13. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
14. Boss BD, Peterson GM, Cowan WM. 1985. On the number of neurons in the dentate gyrus of the rat. Brain Res 338:144-150.
15. Crespo D, Stanfield BB, Cowan WM. 1986. Evidence that late-generated granule cells do not simply replace earlier formed neurons in the rat dentate gyrus. Exp Brain Res 62:541-548.
16. Dolbeare F. 1995. Bromodeoxyuridine: a diagnostic tool in biology and medicine, part I: historical perspectives, histochemical methods and cell kinetics. Histochem J 27:339-369.
17. Eckenhoff MF, Rakic P. 1988. Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. J Neurosci 8:2729-2747.'
18. Edelman G. 1986. Cell adhesion molecules in the regulation of animal form and tissue pattern. Annu Rev Cell Biol 2:81-116.
19. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn A, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nature Med 4:1-5.
20. Gaarskjaer FB. 1986. The organization and development of the hippocampal mossy fiber system. Brain Res 396:335-357.
21. Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, Peterson DA, Suhr ST, Ray J. 1995. Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci USA 92:11879-11883.
22. Gamrani H. Onteniente B, Seguela P, Geffard M, Calas A. 1986. Gamma-aminobutyric acid-immunoreactivity in the rat hippocampus. A light and electron microscopic study with anti-GABA antibodies. Brain Res 364:30-38.
23. Goldman SA, Nottebohm F. 1983. Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci USA 80:2390-394.
24. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS. 1992. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 12:3642-650.
25. Gould E, McEwen BS, Tanapat P, Galea LAM, Fuchs E. 1997. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17:2492-2498.
26. Gratzner HG. 1982. Monoclonal antibody to 5-bromo-and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218: 474-475.
27. Harzsch S, Dawirs RR. 1996. Neurogenesis in the developing crab brain: postembryonic generation of neurons persists beyond metamorphosis. J Neurobiol 29:384-398.
28. Jahn R, Schiebler W, Ouimet C, Greengard P. 1985. A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci USA 82:4137-4141.
29. Kaplan MS, Hinds JW. 1977. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092-1094.
30. Kempermann G, Kuhn HG, Gage FH. 1997a. More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
31. Kempermann G, Kuhn HG, Gage FH. 1997b. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci USA 94:10409-10414.
32. Kempermann G, Kuhn HG, Gage FH. 1998. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18:3206-3212.
33. Kosaka T, Hama K, Yu JY. 1984. GABAergic synaptic boutons in the granule cell layer of rat dentate gyrus. Brain Res 293:353-359.
34. Kuhn HG, Dickinson-Anson H, Gage FH. 1996. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
35. Laatsch RH, Cowan WM. 1966. Electron microscopic studies of the dentate gyrus of the rat. I. Normal structure with special reference to synaptic organization. J Comp Neurol 128:359-395.
36. Lopez-Garcia C, Molowny A, Garcia-Verdugo JM, Ferrer I. 1988. Delayed postnatal neurogenesis in the cerebral cortex of lizards. Brain Res 471:167-174.
37. Markakis EA, Swanson LW. 1997. Spatiotemporal patterns of secretomotor neuron generation in the parvicellular neuroendocrine system. Brain Res Rev 24:255-291.
38. Miller PD, Chung WW, Lagenaur CF, DeKosky ST. 1993. Regional distribution of neural cell adhesion molecule (N-CAM) and L1 in human and rodent hippocampus. J Comp Neurol 327:341-349.
39. Nowakowski RS, Lewin SB, Miller MW. 1989. Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 18:311-318.
40. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH. 1997. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727-3738.
41. Rathjen FG, Schachner M. 1984. Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J 3:1-10.
42. Risold PY, Swanson LW. 1997. Connections of the rat lateral septal complex. Brain Res Rev 24:115-197.
43. Rogers AW. 1973. Technique of autoradiography. Amsterdam: Elsevier.
44. Schlessinger AR, Cowan WM, Gottlieb DI. 1975. An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 159:149-175.
45. Seki T, Arai Y. 1991. The persistent expression of a highly polysialylated NCAM in the dentate gyrus of the rat. Neurosci Res 12:503-513.
46. Seki T, Arai Y. 1993. Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci 13:2351-2358.
47. Simerly RB, Gorski RA, Swanson LW. 1986. Neurotransmitter specificity of cells and fibers in the medial preoptic nucleus: an immunohistochemical study in the rat. J Comp Neurol 246:343-363.
48. Sloviter RS. 1989. Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 280:183-196.
49. Stallcup WB, Beasley LL, Levine JM. 1985. Antibody against nerve growth factor-inducible large external (NILE) glycoprotein labels nerve fiber tracts in the developing rat nervous system. J Neurosci 5:1090-1101.
50. Stanfield BB, Cowan WM. 1979. The development of the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol 185:423-459.
51. Stanfield BB, Trice JE. 1988. Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp Brain Res 72:399-406.
52. Swanson LW. 1992. Brain maps: structure of the rat brain. Amsterdam: Elsevier.
53. Swanson LW. 1993. Brain maps: computer graphics files. Amsterdam: Elsevier.
54. Swanson LW, Sawchenko PE, Cowan WM. 1981. 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 1:548-559.
55. Swanson LW, Kohler C, Bjorklund A. 1987. The limbic region. I: The septohippocampal system. In: Bjorklund A, Hokfelt T, Swanson LW, editors. Handbook of chemical neuroanatomy. Amsterdam: Elsevier. p 125-277.
56. Thomas L, Hartung K, Langosch D, Rehm H, Bamberg E, Franke WW, Betz H. 1988. Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane. Science 242:1050-1053.
57. Wiedenmann B, Franke WW. 1985. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 41:1017-1028.