Skip to main content
Log in

Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections

  • Regular Papers
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

Fully mature rats were injected intraperitoneally with 3H-TdR on postnatal day (P) 100. After an additional 28–32 days, a retrograde fluorescent tracer, either FB or DY, was injected into the regio inferior of the hippocampal formation to label granule cells of the dentate gyrus through their mossy fiber axons. Examination of autoradiographs from these brains reveals that 3H-TdR labeled cells within the granule cell layer of the dentate gyrus are often labeled with the retrograde tracer as well. This indicates that within the mature hippocampal formation, newly generated dentate granule cells are capable of extending axonal projections for considerable distances.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

FB:

fast blue

DY:

diamidino yellow dihydrochloride

3H-TdR:

tritiated thymidine

UV:

ultraviolet

References

  • Altman J (1963) Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec 145: 573–577

    Google Scholar 

  • Altman J, Das G (1965) Autoradiographic and histological evidence of postnatal neurogenesis in rats. J Comp Neurol 124: 319–336

    PubMed  Google Scholar 

  • Angevine JB (1965) Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp Neurol [Suppl] 2, 13: 1–70

    Google Scholar 

  • Avendaño C, Cowan WM (1979) A study of glial cell proliferation in the molecular layer of the dentate gyrus of the rat following interruption of the ventral hippocampal commissure. Anat Embryol 157: 347–366

    Google Scholar 

  • Bayer SA (1980) Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J Comp Neurol 190: 87–114

    Google Scholar 

  • Bayer SA (1982) Changes in the total number of dentate granule cell in juvenile and adult rats: a correlated volumetric and 3Hthymidine autoradiographic study. Exp Brain Res 46: 315–323

    Google Scholar 

  • Bayer SA, Altman J (1974) Hippocampal development in the rat: cytogenesis and morphogenesis examined with autoradiography and low-level X-irradiation. J Comp Neurol 158: 55–80

    Google Scholar 

  • Bayer SA, Yackel JW, Puri PS (1982) Neurons in the rat dentate gyrus granule layer substantially increase during juvenile and adult life. Science 216: 890–892

    Google Scholar 

  • Bentivoglio M, Kuypers HGJM, Catsman-Berrevoets CE, Loewe H, Dann O (1980) Two new fluorescent retrograde tracers which are transported over long distances. Neurosci Lett 18: 25–30

    Google Scholar 

  • Blackstad TW, Brink K, Hem J, Jeune B (1970) Distribution of hippocampal mossy fibers in the rat. An experimental study with silver impregnation methods. J Comp Neurol 138: 433–450

    Google Scholar 

  • Boss BD, Peterson GM, Cowan WM (1985) On the number of neuronal cells in the dentate gyrus of the rat. Brain Res 338: 144–150

    Google Scholar 

  • Cajal SRy (1911) Histologie du système nerveux de l'homme et des vertébrés, Vol 2. Maloine, Paris

    Google Scholar 

  • Claiborne BJ, Amaral DG, Cowan WM (1986) A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J Comp Neurol 246: 435–458

    Google Scholar 

  • Cowan WM, Gottlieb DI, Hendrickson AE, Price JL, Woolsey TA (1972) The autoradiographic demonstration of axonal connections in the central nervous system. Brain Res 37: 21–51

    Google Scholar 

  • Crespo D, Stanfield BB, Cowan WM (1986) Evidence that lategenerated granule cells do not simply replace earlier formed neurons in the rat dentate gyrus. Exp Brain Res 62: 541–548

    Google Scholar 

  • Devor M, Govrin-Lippmann R (1985) Neurogenesis in adult rat dorsal root ganglia. Neurosci Lett 61: 189–194

    Google Scholar 

  • Easter SS (1985) The continuous formation of the retinotectal map in the goldfish, with special attention to the role of the axonal pathway. In: Edelman GM, Gall WI, Cowan WM (eds) Molecular bases of neural development. Wiley, New York, pp 429–452

    Google Scholar 

  • Easter SS, Bratton B, Scherer SS (1984) Growth related order of the retinal fiber layer in goldfish. J Neurosci 4: 2173–2190

    Google Scholar 

  • Gaarskjaer FB (1978) Organization of the mossy fiber system of the rat studied in extended hippocampi. II. Experimental analysis of fiber distribution with silver impregnation methods. J Comp Neurol 178: 73–88

    Google Scholar 

  • Gaarskjaer FB (1981) The hippocampal mossy fiber system of the rat studied with retrograde tracing techniques. Correlation between topographic organization and neurogenetic gradients. J Comp Neurol 203: 717–735

    Google Scholar 

  • Gaarskjaer FB, Laurberg S (1983) Ectopic granule cells of hilus fasciae dentatae projecting to the ipsilateral regio inferior of the rat hippocampus. Brain Res 274: 11–16

    Google Scholar 

  • Gall C, Rose G, Lynch G (1979) Proliferative and migratory activity of glial cells in the partially deafferented hippocampus. J Comp Neurol 183: 539–550

    Google Scholar 

  • 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: 2390–2394

    Google Scholar 

  • Golgi C (1886) Sulla fina anatomia degli organi centrali del sistema nervoso. U Hoepli, Milano, 215 pp

    Google Scholar 

  • Graziadei PPC, Monti Graziadei GA (1978) Continuous nerve cell renewal in the olfactory system. In: Jacobson M (ed) Handbook of sensory physiology, Vol 9. Springer, Berlin Heidelberg New York, pp 55–83

    Google Scholar 

  • Guenéau G, Privat A, Drouet J, Court L (1982) Subgranular zone of the dentate gyrus of young rabbits as a secondary matrix. A high-resolution autoradiographic study. Dev Neurosci 5: 345–358

    Google Scholar 

  • Hübscher U, Kuenzle CC, Spadari S (1979) Functional roles of DNA polymerases-β and-γ. Proc Natl Acad Sci USA 76: 2316–2320

    Google Scholar 

  • Kaplan MS, Bell DH (1983) Neuronal proliferation in the 9-month-old rodent — radioautographic study of granule cells in the hippocampus. Exp Brain Res 52: 1–5

    Google Scholar 

  • Kaplan MS, Bell DH (1984) Miotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J Neurosci 4: 1429–1441

    CAS  PubMed  Google Scholar 

  • Kaplan MS, Hinds JW (1977) Neurogenesis in the adult rat: electron-microscopic analysis of light radioautographs. Science 197: 1092–1094

    Google Scholar 

  • Keizer K, Kuypers HGJM, Huisman AM, Dann O (1983) Diamidino yellow dihydrochloride (DY-2HCl); a new fluorescent retrograde neuronal tracer, which migrates only very slowly out of the cell. Exp Brain Res 51: 179–191

    Google Scholar 

  • Kosaka T (1983) Axon initial segments of the granule cell in the rat dentate gyrus: synaptic contacts on bundles of axon initial segments. Brain Res 274: 129–134

    Google Scholar 

  • Kosaka T (1983) Neuronal gap junctions in the polymorph layer of the rat dentate gyrus. Brain Res 277: 347–351

    Google Scholar 

  • 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: 359–396

    Google Scholar 

  • Lorente de Nó R (1934) Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J Psychol Neurol 46: 113–177

    Google Scholar 

  • Lugaro E (1894) Contributo alla fina anatomia del grande piede d'hippocampo. Arch Scienze Mediche 18: 113–142

    Google Scholar 

  • Paton JA, Nottebohm F (1984) Neurons generated in the adult brain are recruited into functional circuits. Science 225: 1046–1048

    Google Scholar 

  • Paton JA, O'Loughlin BE, Nottebohm F (1985) Cells born in adult canary forebrain are local interneurons. J Neurosci 5: 3088–3093

    Google Scholar 

  • Perone-Capano CG, D'Onofrio G, Giuditta A (1982) DNA turnover in rat cerebral cortex. J Neurochem 38: 52–56

    Google Scholar 

  • Rakic P (1985a) Limits of neurogenesis in primates. Science 227: 1054–1056

    Google Scholar 

  • Rakic P (1985b) DNA synthesis and cell division in the adult primate brain. Ann NY Acad Sci 457: 193–211

    Google Scholar 

  • Rakic P, Nowakowski RS (1981) The time of origin of neurons in the hippocampal region of the rhesus monkey. J Comp Neurol 196: 99–128

    Google Scholar 

  • Rogers AW (1973) Technique of autoradiography, 2nd edn. Elsevier, Amsterdam, 372 pp

    Google Scholar 

  • Sala L (1891) Zur feineren Anatomie des großen Seepferdefußes. Z Wiss Zool 52: 18–45

    Google Scholar 

  • 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: 149–176

    Google Scholar 

  • Stanfield BB, Cowan WM (1979) The development of the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol 185: 423–460

    Google Scholar 

  • Stanfield BB, Cowan WM (1988) The development of the hippocampal region. In: Peters A, Jones EG (eds) Cerebral cortex, Vol 7. The development and maturation of the cerebral cortex. Plenum Press, New York, pp 91–131

    Google Scholar 

  • Swanson LW, Wyss JM, Cowan WM (1978) An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J Comp Neurol 181: 681–716

    Google Scholar 

  • Waser J, Hübscher U, Kuenzle CC, Spadari S (1979) DNA polymerase β from brain neurons is a repair enzyme. Eur J Biochem 97: 361–368

    Google Scholar 

  • Wintzerish M, Witterndorp E, Rechenmann RV, Mandel P (1977) Nuclear, nucleolar repair, or turnover of DNA in adult rat brain. J Neurosci Res 3: 217–230

    Google Scholar 

  • Wyss JM, Sripanidkulchai B (1985) The development of Ammon's horn and the fascia dentata in the cat: A [3H] thymidine analysis. Dev Brain Res 18: 185–198

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stanfield, B.B., Trice, J.E. Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp Brain Res 72, 399–406 (1988). https://doi.org/10.1007/BF00250261

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00250261

Key words

Navigation