Persistent and injury-induced neurogenesis in the vertebrate retina

https://doi.org/10.1016/j.preteyeres.2004.01.001Get rights and content

Abstract

The brains of all vertebrates are persistently neurogenic. However, this is not true for the neural retinas. Only three extant classes of vertebrates show significant posthatch/postnatal retinal neurogenesis: amphibians, birds and fish. The retinas of these animals contain an annulus of progenitors at the margin, from which differentiated neurons emerge. In posthatch amphibians and fish the vast majority of the adult retina is added from the margin and neurogenesis is lifelong, whereas in posthatch birds neurogenesis is limited. Unique to fish, rod photoreceptors are added in situ from stem cells within the mature retina.

Strikingly, for each class of animal retinal lesions stimulate neuronal regeneration, however the cellular source differs for each: the retinal pigmented epithelium in amphibians and embryonic birds, Müller glia in posthatch birds and intrinsic stem cells in fish. The molecular events surrounding injury-induced neuronal regeneration are beginning to be identified.

Section snippets

Introduction: persistent and injury-induced neurogenesis in the retina

The retinas of all vertebrates differentiate from a sheet of multipotent neuroepithelial cells. In mammals, this neuroepithelium is generated through many rounds of cell division in the early embryo, and cells begin to withdraw from the mitotic cell cycle and differentiate in utero or in early postnatal life. The adult complement of retinal neurons is generated in advance of vision and growth of the eye and retina stops at an early point in the animal's lifespan. In contrast, the amphibian and

Neurogenesis in the retinas of amphibians—tadpoles and frogs

The retinas of frogs have been a mainstay in dissecting the cellular and molecular mechanisms that govern neuronal development and differentiation in the nervous system. The first conclusive evidence of neurogenesis at the margin of a vertebrate retina was gained from studies using tadpoles (Hollyfield, 1968; Straznicky and Gaze, 1971). Following an intravitreal injection of 3H-thymidine to label dividing cells and short survival times, the 3H-label was found in spindle-shaped, undifferentiated

Injury-induced neurogenesis in the retina: models of CNS repair

A hallmark of the central nervous system in most adult vertebrates, certainly all adult mammals, is that significant injuries are not repaired and capacities lost through neuronal death are not regained. With the growth of our knowledge concerning neural stem cells, it is hoped that a therapeutic cellular treatment for brain injuries might one day be realized. This is a particularly attractive strategy in the retina where the major blinding diseases impact a limited number of cell types. It is

Finale

Understanding the cellular mechanisms that regulate developmental and regenerative neurogenesis has been a subject of intense interest among neurobiologists for decades. This review has focused on our current knowledge of these processes in the retinas of amphibians, birds and fish. While intriguing in their own right, comparative studies may provide the basis for understanding mechanisms regulating neurogenesis in the mammalian retina and insights into the potential for and limitations of

Acknowledgements

The authors thank Laura Kakuk-Atkins and Randall Wallach and Drs. Deborah Stenkamp and Philip Gage for reading and commenting on preliminary versions of this paper. Preparation of this review was funded in part by NIH grants R01-EY07060 (PH), P30-EY07003 (PH), T32-EY013934 (MO), T32-DC05341 (AS) and F32-EY13499 (DO).

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