Number, distribution, and morphology of retinal ganglion cells with axons regenerated into peripheral nerve graft in adult cats

The optic nerve of adult cats was transected and an autologous peripheral nerve was transplanted to the stump. Two months later retinal ganglion cells (RGCs) that had regenerated their axons were retrogradely labeled with fluorescent dye injected into the graft. The more than 4000 labeled cells, which were 3.0–4.3% of total ganglion cell number in the intact retina, were distributed in a high-density area elongating horizontally, in a pattern similar to that observed in the intact retina. The dendritic morphology of RGCs with regenerated axons was examined after intracellular injections of HRP or Lucifer yellow in vitro. The morphology of alpha- and gamma-cells appeared comparable to normal, whereas the dendrites of some beta-cells seemed to degenerate. Some “unclassified” cells could not be identified as alpha-, beta-, or gamma-cells. The main dendrites of most unclassified cells were thin and less ramified than alpha- and beta-cells. Some unclassified cells had a vacant area in their dendritic fields, suggesting degenerative change in dendrites. The distal dendrites of some unclassified and gamma-cells had many fine processes that probably regrew during axonal regeneration. The proportion of alpha-, beta-, and other cells including gamma- and unclassified cells in the regenerating cell population was evaluated by examining all of the Lucifer yellow- injected cells in local patches. The average proportion of alpha-cells was 23.9%, about six times higher than in intact retinas. The average proportion of beta-cells was 50.3%, slightly higher than in intact retinas. The remaining cells (25.7%) could not be categorized as alpha or beta; this proportion is about half that found in intact retinas. These findings suggest that alpha-cells have the highest capacity to regenerate their axons into nerve grafts, rather than all types equally regenerating their axons.

[1]  D. Carter,et al.  Regenerated retinal ganglion cell axons can form well-differentiated synapses in the superior colliculus of adult hamsters , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  B. Boycott,et al.  The morphological types of ganglion cells of the domestic cat's retina , 1974, The Journal of physiology.

[3]  P. O. Bishop,et al.  Some quantitative aspects of the cat's eye: axis and plane of reference, visual field co‐ordinates and optics , 1962, The Journal of physiology.

[4]  A Hughes,et al.  Population magnitudes and distribution of the major modal classes of cat retinal ganglion cell as estimated from HRP filling and a systematic survey of the soma diameter spectra for classical neurones , 1981, The Journal of comparative neurology.

[5]  Y. Fukuda,et al.  Morphological correlates of physiologically identified Y-, X-, and W-cells in cat retina. , 1984, Journal of neurophysiology.

[6]  R. W. Rodieck,et al.  Parasol and midget ganglion cells of the human retina , 1985, The Journal of comparative neurology.

[7]  R. Williams,et al.  Binocular interaction in the fetal cat regulates the size of the ganglion cell population , 1984, Neuroscience.

[8]  H. Wässle,et al.  The cat optic nerve: Fibre total count and diameter spectrum , 2004, The Journal of comparative neurology.

[9]  A Hughes,et al.  A quantitative analysis of the cat retinal ganglion cell topography , 1975, The Journal of comparative neurology.

[10]  H. Spekreijse,et al.  Visual Pathways , 1981, Documenta Ophthalmologica Proceedings Series.

[11]  J. Stone,et al.  Properties of cat retinal ganglion cells: a comparison of W-cells with X- and Y-cells. , 1974, Journal of neurophysiology.

[12]  S. Sherman,et al.  Structure/function relationships of retinal ganglion cells in the cat , 1984, Brain Research.

[13]  Y. Fukuda,et al.  The relation between axon diameter and axonal conduction velocity of Y, X and W cells in the cat retina , 1984, Brain Research.

[14]  J. Stone,et al.  Correlation between soma size and dendritic morphology in cat retinal ganglion cells: Evidence of further variation in the γ‐cell class , 1980, The Journal of comparative neurology.

[15]  H. Wässle,et al.  The distribution of the alpha type of ganglion cells in the cat's retina , 1975, The Journal of comparative neurology.

[16]  H. Saito,et al.  Morphology of physiologically identified X‐, Y‐, and W‐type retinal ganglion cells of the cat , 1983, The Journal of comparative neurology.

[17]  S. Thanos,et al.  Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  B. Boycott,et al.  Morphology and topography of on- and off-alpha cells in the cat retina , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[19]  W. Levick,et al.  Brisk and sluggish concentrically organized ganglion cells in the cat's retina , 1974, The Journal of physiology.

[20]  R H Masland,et al.  The shape and arrangement of the cholinergic neurons in the rabbit retina , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[21]  R. W. Rodieck,et al.  Parasol and midget ganglion cells of the primate retina , 2004 .

[22]  Y. Fukuda,et al.  Axonal regeneration of retinal ganglion cells in the cat geniculocortical pathway , 1991, Brain Research.

[23]  J. Stone,et al.  Estimate of the number of myelinated axons in the cat's optic nerve , 1978, The Journal of comparative neurology.

[24]  K. So,et al.  Lengthy regrowth of cut axons from ganglion cells after peripheral nerve transplantation into the retina of adult rats , 1985, Brain Research.

[25]  J. Stone,et al.  Retinal distribution and central projections of Y-, X-, and W-cells of the cat's retina. , 1974, Journal of neurophysiology.

[26]  R. Williams,et al.  An analysis of axon caliber within the optic nerve of the cat: evidence of size groupings and regional organization , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  Y. Fukuda Axonal regeneration of cat retinal ganglion cells after peripheral nerve transplant , 1991 .

[28]  B. Boycott,et al.  Alpha ganglion cells in mammalian retinae , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.