Summary
In the albino rat, the number of optic axons increases from 400 on embryonic day 15 to reach a peak of 240000 at birth, before declining to adult numbers (100000) by postnatal day 5. Throughout the period of loss of axons there are few signs of degeneration in the optic nerve, which does not change its diameter: the decrease in density of axons is matched by an increase in the cross-sectional area of individual axons. Myelination of the initially non-myelinated axons starts on day 5, when axonal numbers stabilize. Following neonatal removal of one eye, fewer axons than normal are present in the contralateral optic nerve up to day 5. The axons removed by enucleation may be retino-retinal axons, representing up to 40% of the 83000 fibres lost between postnatal days 2 and 5. There is no increase in the numbers of optic axons in the remaining nerve in adult animals; this appears to be due to the small absolute numbers of ipsilateral axons saved by enucleation. After enucleation, axons remain clear and undergo a “watery” degeneration after initially swelling, and the removal of degenerative products is accomplished within four days.
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References
Arneson AR, Osen KK, Mugnaini E (1978) Temporal and spatial sequence of anterograde degeneration in the cochlear nerve fibers of the cat. A light microscopic study. J Comp Neurol 178: 679–696
Baisinger J, Lund RD, Miller B (1977) Aberrant retino-thalamic projections resulting from unilateral tectal lesions made in fetal and neonatal rats. Exp Neurol 54: 369–382
Berger B (1971) Etude ultrastructurale de la degenerescence Wallerienne experimentale d'un nerf entirement amyelinique: le nerf olfactif. 1. Modifications axonales. Ultrastruct Res 37: 105–118
Bignami MD, Dahl D, Nguyen BT, Crosby CJ (1981) The fate of axonal debris in Wallerian degeneration of rat optic and sciatic nerves. J Neuropath Exp Neurol 40: 537–550
Bunt SM, Lund RD (1981) Development of a transient retinoretinal pathway in hooded and albino rats. Brain Res 211: 399–404
Bunt S, Lund RD, Land P (1983) Prenatal development of the optic projection in albino and hooded rats. Dev Brain Res 6: 149–168
Chu-Wang I-W, Oppenheim RW (1978) A quantitative and qualitative analysis of degeneration in the ventral root, including evidence for axon outgrowth and limb innervation prior to cell death. J Comp Neurol 177: 59–86
Clarke PGH, Rogers LA, Cowan WM (1976) The time of origin and the pattern of survival of neurons in the isthmo-optic nucleus in the chick. J Comp Neurol 167: 125–142
Clifton GL, Vance WH, Applebaum ML, Coggeshall RE, Willis WD (1974) Responses of unmyelinated afferents in the mammalian ventral root. Brain Res 82: 163–167
Cook RD, Ghetti B, Wisniewski HM (1974) The pattern of Wallerian degeneration in the optic nerve of newborn kittens: an ultrastructural study. Brain Res 75: 261–275
Cowan WM (1979) Selection and control in neurogenesis. In: Schmitt FO, Worden FG (ed) The neurosciences fourth study program. MIT Press, Cambridge, pp 59–79
Cunningham TJ, Mohler IM, Giordano DL (1981) Naturally occurring neuron death in the ganglion cell layer of the neonatal rat: morphology and evidence for regional correspondence with neuron death in superior colhculus. Dev Brain Res 2: 203–215
DeJuan J, Iniguez C, Carreres J (1978) Number, diameter and distribution of the rat optic nerve fibres. Acta Anat 102: 294–299
Dreher B, Potts RA, Bennett MR (1983) Evidence that the early postnatal reduction in the number of rat retinal ganglion cells is due to a wave of ganglion cell death. Neurosci Lett 36: 255–260
Dreher B, Potts RA, Ni SYK, Bennett MR (1984) The development of heterogeneities in distribution and soma sizes of rat retinal ganglion cells. In: Stone J, Dreher B, Rapaport DH (ed) Development of visual pathways in mammals. Alan R. Liss, New York, pp 39–58
Finlay BL, Wilson KG, Schneider GE (1979) Anomalous ipsilateral retinotectal projections in Syrian hamsters with early lesions: topography and functional capacity. J Comp Neurol 183: 721–740
Forrester J, Peters A (1967) Nerve fibres in optic nerve of rat. Nature 214: 245–247
Foster RE, Connors BW, Waxman SG (1982) Rat optic nerve: electrophysiological, pharmacological and anatomical studies during development. Dev Brain Res 3: 371–386
Frost DO, So K-F, Schneider GE (1979) Postnatal development of retinal projections in Syrian hamsters: a study using autoradiographic and anterograde degeneration techniques. J Neurosci 4: 1649–1677
Fukuda Y, Sugimoto T, Shirokawa T (1982) Strain differences in quantitative analysis of the rat optic nerve. Exp Neurol 75: 525–532
Giordano DL, Murray M, Cunningham TJ (1980) Naturally occurring cell death in the optic layers of superior colliculus of the postnatal rat. J Neurocyt 9: 603–614
Heumann D, Rabinowitz T (1980) Postnatal development of the dorsal lateral geniculate nucleus in the normal and enucleated albino mouse. Exp Brain Res 38: 75–85
Hughes A (1977) The pigmented-rat optic nerve: fibre count and fibre diameter spectrum. J Comp Neurol 176: 263–268
Hughes WF, LaVelle A (1975) Effects of early tectal lesions on development in retinal ganglion cell layer of chick embryos. J Comp Neurol 163: 265–284
Hughes WF, McLoon SC (1979) Ganglion cell death during normal retinal development in the chick: comparisons with cell death induced by early target field destruction. Exp Neurol 66: 587–601
Insausti R, Blakemore C, Cowan WM (1984) Ganglion cell death during development of ipsilateral retino-collicular projection in golden hamster. Nature (London) 308: 362–365
Jeffery G, Perry VH (1981) Evidence for ganglion cell death during development of the ipsilateral retinal projection in the rat. Dev Brain Res 2: 176–180
Jen L-S, Lund RD (1979) Intertectal crossing of optic axons after tectal fusion in neonatal rats. Brain Res 178: 99–105
Jen L-S, Lund RD (1981) Experimentally induced enlargement of the uncrossed retinotectal pathway in rats. Brain Res 211: 37–57
Karlsson U (1967) Observations on the postnatal development of neuronal structures in the lateral geniculate nucleus of the rat by electron microscopy. J Ulstrastruct Res 17: 158–175
Kuwabara T (1975) Development of the optic nerve of the rat. Invest Ophthalmol 14: 732–745
Laemle LK, Labriola AR (1982) Retinocollicular projections in the neonatal rat: an anatomical basis for plasticity. Dev Brain Res 3: 317–322
Lam K, Sefton AJ, Bennett MR (1982) Loss of axons from the optic nerve of the rat during early postnatal development. Dev Brain Res 3: 387–491
Land PW, Lund RD (1979) Development of the rat's uncrossed retinotectal pathway and its relation to plasticity studies. Science 205: 698–700
Lieberman AR (1974) Some factors affecting retrograde neuronal responses to axonal lesions. In: Bellairs R, Gray EG (ed) Essays on the nervous system. Clarendon, Osford, p 71–105
Lund RD (1965) Uncrossed visual pathways of hooded and albino rats. Science 149: 1506–1507
Lund RD, Land PW, Boles J (1980) Normal and abnormal uncrossed retinotectal pathways in rats: an HRP study in adults. J Comp Neurol 189: 711–720
Lund RD, Lund JS (1971) Modifications of synaptic patterns in the superior colliculus of the rat during development and following deafferentation. Vis Res Suppl 3: 281–298
Lund RD, Miller BF (1975) Secondary effects of fetal eye damage in rats on intact central optic projections. Brain Res 92: 279–289
McCaffery CA, Bennett MR, Dreher B (1982) The survival of neonatal rat retinal ganglion cells in vitro is enhanced in the presence of appropriate parts of the brain. Exp Brain Res 48: 377–386
Martin PR, Sefton AJ, Dreher B (1983) The retinal location and fate of ganglion cells which project to the ipsilateral superior colliculus in neonatal albino and hooded rats. Neurosci Lett 41: 219–226
Miller NM, Oberdorfer M (1981) Neuronal and neuroglial responses following retinal lesions in the neonatal rats. J Comp Neurol 202: 493–504
Ng AYK, Stony J (1982) The optic nerve of the cat: appearance and loss of axons during normal development. Dev Brain Res 5: 263–271
Nurcombe V, Bennett MR (1981) Embryonic chick retinal ganglion cells identified “in vitro”. Their survival is dependent on a factor from the optic tectum. Exp Brain Res 44: 249–258
Pecci-Saavedra J, Mascitti TA, Lloret LP (1973) Increased rate of anterograde degeneration in the visual pathway of kittens. Brain Res 50: 265–274
Perry VH, Cowey A (1979) Changes in the retino-fugal pathways following cortical and tectal lesions in neonatal and adult rats. Exp Brain Res 35: 97–108
Perry VH, Cowey A (1982) A sensitive period for ganglion cell degeneration and the formation of aberrant retino-fugal connections following tectal lesions in rats. Neuroscience 7: 583–594
Perry VH, Henderson Z, Linden R (1983) Postnatal changes in retinal ganglion cell and optic axon populations in the pigmented rat. J Comp Neurol 219: 356–368
Polyak S (1957) The vertebrate visual system. University of Chicago Press, Chicago, p 315
Potts RA, Dreher B, Bennett MR (1982) The loss of ganglion cells in the developing retina of the rat. Dev Brain Res 3: 481–486
Rager G (1980) Development of the retinotectal projection in the chicken. Adv Anat Embryol Cell Biol 63: 1–92
Rager G, Rager U (1978) Systems-matching by degeneration I. A quantitative electron microscopic study of the generation and degeneration of retinal ganglion cells in the chicken. Exp Brain Res 33: 65–78
Rakic P, Riley KP (1983) Regulation of axon number in primate optic nerve by prenatal binocular competition. Nature 305: 135–137
Sakai M, Yagi F (1981) Evoked potential in the lateral geniculate body as modified by enucleation of one eye in the albino rat. Brain Res 210: 91–102
Schneider GE (1973) Early lesions of superior colliculus: factors affecting the formation of abnormal retinal projections. Brain Behav Evol 8: 73–109
Sengelaub DR, Finlay BL (1981) Early removal of one eye reduces normally occurring cell death in the remaining eye. Science 213: 573–574
Sengelaub DR, Finlay BL (1982) Cell death in the mammalian visual system during normal development: I. Retinal ganglion cells. J Comp Neurol 204: 311–317
Shirokawa T, Fukuda Y, Sugimoto T (1983) Bilateral reorganization of the rat optic tract following enucleation of one eye at birth. Exp Brain Res 51: 172–178
Silver J, Shapiro J (1981) Axonal guidance during development of the optic nerve: the role of pigmented epithelia and other factors. J Comp Neurol 202: 521–538
Skoff RP, Price DL, Stocks A (1976) Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve I. Time of origin. J Comp Neurol 169: 313–334
Skoff RP, Toland D, Nast E (1980) Pattern of myelination and distribution of neuroglial cells along the developing optic system of the rat and rabbit. J Comp Neurol 191: 237–253
So K-F (1979) Development of abnormal recrossing retinotectal projections after superior colliculus lesions in newborn Syrian hamsters. J Comp Neurol 186: 241–258
Stevenson JA, Lund RD (1982) A crossed parabigemino-lateral geniculate projection in rats blinded at birth. Exp Brain Res 45: 95–100
Treff WM, Meyer-Konig E, Schlote W (1972) Morphometric analysis of a fibre system in the central nervous system. J Microsc 95:, 337–343
Udin SB, Schneider GE (1981) Compressed retinotectal projection in hamsters: fewer ganglion cells project to tectum after neonatal tectal lesions. Exp Brain Res 43: 261–269
Vaughn JE (1969) An electron microscopic analysis of gliogenesis in rat optic nerves. Z Zellforsch 94: 293–324
Weedon D, Searle J, Kerr JFR (1979) Apoptosis. Its nature and implications for dermatopathology. Am J Dermatopath 1: 133–144
Wiedman TA, Kuwabara T (1968) Postnatal development of the rat retina. Arch Ophthalmol 79: 470–484
Williams RW, Bastiani MJ, Chalupa LM (1983) Loss of axons in the cat optic nerve following fetal unilateral enucleation: an electron microscopic analysis. J Neurosci 3: 133–144
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Sefton, A.J., Lam, K. Quantitative and morphological studies on developing optic axons in normal and enucleated albino rats. Exp Brain Res 57, 107–117 (1984). https://doi.org/10.1007/BF00231137
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DOI: https://doi.org/10.1007/BF00231137