Retinal ganglion cell death during optic nerve regeneration in the frog <i>hyla moorei</i>

Humphrey, M.F.; Beazley, Lyn

doi:10.1002/cne.902360307

Cited by 82 publications

(114 citation statements)

References 46 publications

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“…However, there were two clear abnormalities. One was that, as in frogs with regenerated optic nerves (Humphrey and Beazley, 1985;Humphrey et al, 1992), the tectal input no longer formed distinct laminae (Fig. 5B).…”

Section: Anatomymentioning

confidence: 96%

“…Thus, in fish, almost the entire retinal ganglion cell population survives axotomy and undergoes axonal regeneration (Marotte et al, 1979;Murray et al, 1982). In the class more recently evolved than fish, the amphibians, only between 50-70% of ganglion cells survive axotomy (Beazley, 1981;Humphrey and Beazley, 1985;Scalia et al, 1985;Stelzner and Strauss, 1986;Beazley et al, 1986;Humphrey, 1987Humphrey, , 1988Humphrey et al, 1989;Singman and Scalia, 1991;Beazley and Darby, 1993).…”

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confidence: 99%

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Optic nerve regenerates but does not restore topographic projections in the lizardCtenophorus ornatus

et al. 1997

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In adult fish and amphibians, the severed optic nerve regenerates and visual behaviour is restored. By contrast, optic axons do not regenerate in the more recently evolved birds and mammals. Here we have investigated optic nerve regeneration in a member of the class Reptilia, phylogenetically intermediate between the fish and amphibians and the birds and mammals. We assessed visual recovery anatomically and behaviourally one year after unilateral optic nerve crush in the adult ornate dragon lizard. Ctenophorus ornatus. Ganglion cell densities and numbers of axons in the optic nerve on either side of the crush site indicated that two-thirds of ganglion cells survived axotomy and regrew their axons. However, myelination fell from a mean of 21% in normals to 5.5% and 3%, proximal and distal to the crush, respectively. Anterograde labelling of the entire optic nerve showed that axons regenerated along essentially normal pathways and that the major projection, as in normals, was to the superficial one-third of the contralateral optic tectum. However, localised retinal injections indicated that regenerated projections lacked retinotopic order. Any one retinal region projected to the entire tectum. This feature presumably explains why the experimental lizards consistently appeared blind to stimuli via the regenerated nerve. Our findings indicate that although axons regenerate along essentially normal pathways in adult lizards, conditions within the visual centres do not allow regenerating optic axons to select appropriate central connections. In a wider context, the result suggests that the ability for regenerating central axons to form topographic maps may also have been lost in the more recently evolved vertebrate classes.

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Section: Anatomymentioning

confidence: 96%

mentioning

confidence: 99%

Optic nerve regenerates but does not restore topographic projections in the lizardCtenophorus ornatus

et al. 1997

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“…Intriguingly, in adult amphibia, optic nerve axotomy induces cell death in approximately 40-70% of the RGCs, yet, the surviving RGCs partially or even fully regenerate and connect with their targets in the optic tectum (Humphrey and Beazley 1985;Beazley et al 1986;Soto et al 2003;Duprey-Diaz et al 2016). The time course and spatial distribution of regenerating axons after optic nerve injury is well-characterized.…”

Section: Models and Methods To Study Spontaneous Optic Nerve Regeneramentioning

confidence: 99%

Complementary research models and methods to study axonal regeneration in the vertebrate retinofugal system

et al. 2017

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Due to the lack of axonal regeneration, age-related deterioration in the central nervous system (CNS) poses a significant burden on the wellbeing of a growing number of elderly. To overcome this regenerative failure and to improve the patient's life quality, the search for novel regenerative treatment strategies requires valuable (animal) models and techniques. As an extension of the CNS, the retinofugal system, consisting of retinal ganglion cells that send their axons along the optic nerve to the visual brain areas, has importantly contributed to the current knowledge on mechanisms underlying the restricted regenerative capacities and to the development of novel strategies to enhance axonal regeneration. It provides an extensively used research tool, not only in amniote vertebrates including rodents, but also in anamniote vertebrates, such as zebrafish. Indeed, the latter show robust regeneration capacities, thereby providing insights into the factors that contribute to axonal regrowth and proper guidance, complementing studies in mammals. This review provides an integrative and critical overview of the classical and state-of-the-art models and methods that have been employed in the retinofugal system to advance our knowledge on the signaling pathways underlying the restricted versus robust axonal regeneration in rodents and zebrafish, respectively. In vitro, ex vivo and in vivo models and techniques to improve the visualization and analysis of regenerating axons are summarized. As such, the retinofugal system is presented as a valuable model to further facilitate research on axonal regeneration and to open novel therapeutic avenues for CNS pathologies.

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“…As the great majority of neurons in the ganglion cell layer of frogs are RGCs Humphrey and Beazley, 1985], it seems likely that many of these dying cells are RGCs rather than displaced amacrine cells. Second, follow ing optic nerve crushes in the adults of two anuran species [Hyla moorei: Humphrey and Beazley, 1985;Rana pipiens: Beazley et al, 1985], there is a delayed wave of RGC death in which 40-50% of RGCs are eli minated. If this elimination is related to the refine ment of the re-established retinotectal projection (as Beazley et al suggest), then it seems quite likely that RGC death also occurs during the refinement of the normal retinofugal pathway.…”

Section: Phylogeny Of Temporal Matchingmentioning

confidence: 99%

“…First, substantial numbers of pyknotic profiles have been observed in the developing ganglion cell layer of the X. laevis tad pole [Gliicksmann, 1965]. As the great majority of neurons in the ganglion cell layer of frogs are RGCs Humphrey and Beazley, 1985], it seems likely that many of these dying cells are RGCs rather than displaced amacrine cells. Second, follow ing optic nerve crushes in the adults of two anuran species [Hyla moorei: Humphrey and Beazley, 1985;Rana pipiens: Beazley et al, 1985], there is a delayed wave of RGC death in which 40-50% of RGCs are eli minated.…”

Section: Phylogeny Of Temporal Matchingmentioning

confidence: 99%

Development of the Retinofugal Pathway in Birds and Mammals: Evidence for a common 'timetable'. (Part 2 of 2)

Dreher¹,

Robinson²

1988

Brain Behav Evol

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We have compared changes in axon numbers in the developing optic nerves of eight homeotherms (seven mammals and one bird) using data from the available literature and our own material. The proportion of axons lost during development is smaller in the chick (35%) than in mammals (54–74%). The relative magnitude of this loss does not correlate with the extent of the binocular visual field or the size of the retinofugal ipsilateral projection. The timing of developmental events in the retinofugal pathway was compared as a proportion of the period between conception and eye opening (percentage of the 'caecal period', CP). In eutherian mammals, retinal ganglion cells and their target neurons are generated between 30 and 49% of CP (a duration of 19% of CP). In homeotherms, a phase of rapid axon generation begins around 38% of CP and the peak number of axons is reached at about 56 % of CP (a duration of 18 % of CP). A phase of rapid axon loss begins thereafter, and in most species it ends at about 74% of CP (a duration of 18% of CP), the rate of rapid axons loss being about half the rate of rapid axon generation. The similarity in relative timing (homochrony), like the similarity in the relative magnitude of the axon loss, suggests that cell generation and loss in the retinofugal pathway are influenced by a mechanism common to all homeotherms. We propose that in homeotherms each cohort of retinal ganglion cells is numerically matched with a group of target cells that is at an appropriate stage of maturation ('temporal matching' hypothesis). About twice as many ganglion cells are produced in each cohort than are needed, and their survival is determined by natural selection.

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Retinal ganglion cell death during optic nerve regeneration in the frog hyla moorei

Cited by 82 publications

References 46 publications

Optic nerve regenerates but does not restore topographic projections in the lizardCtenophorus ornatus

Optic nerve regenerates but does not restore topographic projections in the lizardCtenophorus ornatus

Complementary research models and methods to study axonal regeneration in the vertebrate retinofugal system

Development of the Retinofugal Pathway in Birds and Mammals: Evidence for a common 'timetable'. (Part 2 of 2)

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