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PMID: 7638182 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Intrinsic changes in developing retinal neurons result in regenerative failure of their axons.

Chen DF, Jhaveri S, Schneider GE

Abstract

The failure of mature mammalian central nervous system axons to regenerate after transection is usually attributed to influences of the extraneuronal milieu. Using explant cocultures of retina and midbrain tectum from hamsters, we have found evidence that these influences account for failure of regrowth of only a small minority of retinal axons. For most of the axons, there is a programmed loss of ability to elongate in the central nervous system. We show that there is a precipitous decline in the ability of retinal axons to reinnervate tectal targets when the retina is derived from pups on or after postnatal day 2, even when the target is embryonic. By contrast, embryonic retinal axons can regrow into tectum of any age, overcoming growth-inhibiting influences of glial factors.

MeSH Terms
Age Factors Animals Axons/physiology Cricetinae Culture Techniques Mesocricetus Nerve Regeneration/physiology Oligodendroglia/cytology Retina/cytology,embryology,growth & development Superior Colliculi/cytology,embryology,growth & development Visual Pathways/cytology,embryology,growth & development
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Chen D F
Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge 02139, USA.
Jhaveri S
Schneider G E
References (32)
32 references, click to expand
  1. Lesions of the brachium of the superior colliculus in neonate hamsters: correlation of anatomy with behavior.
    Exp Neurol. 1981 May;72(2):379-400 PMID: 7238698
  2. Neurobiology. Inhibitory influences.
    Nature. 1994 Oct 20;371(6499):658-9 PMID: 7523955
  3. Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures.
    J Cell Biol. 1986 Jul;103(1):171-87 PMID: 2424918
  4. Control of cell number in the developing visual system. II. Effects of partial tectal ablation.
    Brain Res. 1986 Jul;393(1):11-21 PMID: 3730888
  5. Retinal ganglion cells lose response to laminin with maturation.
    Nature. 1986 Jul 31-Aug 6;322(6078):465-7 PMID: 2874498
  6. The postnatal development of the optic nerve in hamsters: an electron microscopic study.
    Brain Res. 1986 Dec;395(2):268-73 PMID: 3779443
  7. Retinal ganglion cell survival and neurite regeneration requirements: the change from Müller cell dependence to superior colliculi dependence during development.
    Brain Res. 1987 Apr;429(2):207-16 PMID: 3552123
  8. The role of laminin and the laminin/fibronectin receptor complex in the outgrowth of retinal ganglion cell axons.
    Dev Biol. 1987 Aug;122(2):407-18 PMID: 2954871
  9. Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat.
    J Neurosci. 1987 Sep;7(9):2894-909 PMID: 3625278
  10. Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats.
    J Neurosci. 1988 Jan;8(1):265-80 PMID: 2448429
  11. Changes in rapidly transported proteins in developing hamster retinofugal axons.
    J Neurosci. 1988 Dec;8(12):4445-54 PMID: 3199185
  12. Intrinsic differences in the growth rate of early nerve fibres related to target distance.
    Nature. 1989 Feb 9;337(6207):553-5 PMID: 2915705
  13. Cellular organization and development of slice cultures from rat visual cortex.
    Exp Brain Res. 1989;77(2):234-44 PMID: 2477270
  14. Immunohistochemical localization of GAP-43 in the developing hamster retinofugal pathway.
    J Comp Neurol. 1989 Oct 1;288(1):51-8 PMID: 2794137
  15. In situ demonstration of mature oligodendrocytes and their processes: an immunocytochemical study with a new monoclonal antibody, rip.
    Glia. 1989;2(5):380-90 PMID: 2530173
  16. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors.
    Nature. 1990 Jan 18;343(6255):269-72 PMID: 2300171
  17. Directed early axonal outgrowth from retinal transplants into host rat brains.
    J Neurobiol. 1990 Dec;21(8):1202-18 PMID: 2177099
  18. Laminin receptors in the retina: sequence analysis of the chick integrin alpha 6 subunit. Evidence for transcriptional and posttranslational regulation.
    J Cell Biol. 1991 Apr;113(2):405-16 PMID: 1826298
  19. Tumor necrosis factor facilitates regeneration of injured central nervous system axons.
    Brain Res. 1991 Apr 5;545(1-2):334-8 PMID: 1860055
  20. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes.
    J Neurosci. 1991 Nov;11(11):3398-411 PMID: 1719160
  21. Regenerating adult rat retinal axons reconnect with target neurons in-vitro.
    Neuroreport. 1991 Oct;2(10):581-4 PMID: 1661620
  22. Axonal regeneration of retinal ganglion cells in the cat geniculocortical pathway.
    Brain Res. 1991 Sep 27;560(1-2):330-3 PMID: 1760740
  23. Initial stages of retinofugal axon development in the hamster: evidence for two distinct modes of growth.
    Exp Brain Res. 1991;87(2):371-82 PMID: 1722759
  24. Intrinsic neuronal determinants of regeneration.
    Trends Neurosci. 1992 Jan;15(1):5-8 PMID: 1374956
  25. Laminar specificity of extrinsic cortical connections studied in coculture preparations.
    Neuron. 1992 Aug;9(2):217-28 PMID: 1497891
  26. Mechanisms governing neuronal degeneration and axonal regeneration in the mature retinofugal system.
    J Cell Sci Suppl. 1991;15:125-34 PMID: 1824103
  27. Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus.
    Neuron. 1992 Oct;9(4):643-56 PMID: 1389181
  28. Oligodendrocytes and myelin formation along the optic tract of the developing hamster: an immunohistochemical study using the Rip antibody.
    Glia. 1992;6(2):138-48 PMID: 1398895
  29. Long-term growth and remodeling of regenerated retino-collicular connections in adult hamsters.
    J Neurosci. 1994 Feb;14(2):590-8 PMID: 7507980
  30. [Experimental evidence that endogenous TSH modulates microsomal antigen expression: clinical implications].
    Rev Med Chil. 1993 Oct;121(10):1099-104 PMID: 8191112
  31. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration.
    Neuron. 1994 Sep;13(3):757-67 PMID: 7522484
  32. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats.
    Science. 1981 Nov 20;214(4523):931-3 PMID: 6171034
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1995-08-01
Pages
7287-91
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC41324
Subset
IM
Grants
NEI NIH HHS · EY00126 · United States
NEI NIH HHS · EY02621 · United States
NEI NIH HHS · EY05504 · United States
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