Elsevier

Experimental Neurology

Volume 66, Issue 3, December 1979, Pages 587-601
Experimental Neurology

Ganglion cell death during normal retinal development in the chick: Comparisons with cell death induced by early target field destruction

https://doi.org/10.1016/0014-4886(79)90204-8Get rights and content

Abstract

Ganglion cell death during normal retinal development in the chick was observed in retinal whole mounts and in specimens sectioned for light and electron microscopy. Pyknotic cells were observed between the 12th and 16th days of incubation. These accounted for the loss of at least 20% of the cells from the ganglion cell layer. Early destruction of the primordial optic tectum produced an increased degeneration of ganglion cells (72%) during this same critical period when they evidently became dependent on central associations. Death of ganglion cells at this time in normal development suggests that significant numbers may ordinarily be unable to form sustaining connections. Normal and experimentally induced cell death immediately preceded a phase of cytological maturation which was generally evident in the ganglion cell layer by the 15th day of incubation. Developments with respect to the target field may not only maintain the cell but actually influence its late maturation. Counts from selected regions of retinal whole mounts revealed an overall temporal to nasal progression of cell death. This pattern was also seen in retinae when the tectum had been destroyed early in development. The pattern, therefore, was not regulated by interactions with target field, suggesting that ganglion cells in early phases of development proceed according to an intrinsic retinal program. The temporal to nasal retinal sequence, although independent of the tectum, appears to correspond to the progress of maturation in retinotopically related regions of the tectum. Coincident developments in the two fields could contribute to the retinotopic organization of the visual projection on region to region basis.

References (34)

  • W.M. Cowan et al.

    Mitotic patterns in the optic tectum of the chick during normal development and after early removal of the optic vesicle

    J. Exp. Zool.

    (1968)
  • W.M. Cowan et al.

    Cell loss in the trochlear nucleus of the chick during normal development and after radical extirpation of the optic vesicle

    J. Exp. Zool.

    (1977)
  • W.J. Crossland et al.

    Specification of the retino-tectal projection in the chick

    J. Comp. Neurol.

    (1974)
  • S. Goldberg et al.

    Topographical development of the ganglion cell fiber layer in the chick retina. A whole mount study

    J. Comp. Neurol.

    (1972)
  • A. Glücksmann

    Development and differentiation of tadpole eye

    Br. J. Ophthalmol.

    (1940)
  • A. Glücksmann

    Cell deaths in normal vertebrate ontogeny

    Biol. Rev.

    (1951)
  • V. Hamburger

    The effects of wing bud extirpation on the development of the central nervous system in chick embryos

    J. Exp. Zool.

    (1934)
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    1

    This work was supported by Special Visual Sciences Award NIH-EY-01477-03 to W.F.H., the Helen Regenstein Foundation, and the Louise Norton Trust.

    2

    This paper is, in part, based on a dissertation by Dr. McLoon in partial fulfillment of his requirements for the Ph.D. degree at the University of Illinois Medical Center. Dr. McLoon's present address is the Department of Anatomy, Medical University of South Carolina, 171 Ashley, Charleston, South Carolina, 29403. The authors wish to thank Mrs. Joana Aras for technical assistance and Mrs. Mary Dever for typing the final manuscript.

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