Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat

In adult rats, one optic nerve was transected and replaced by a 4 cm segment of autologous peripheral nerve (PN) that linked one eye and the superior colliculus (SC) along a predominantly extracranial course. Retrograde and orthograde studies with the tracers HRP or rhodamine-B- isothiocyanate (RITC), as well as immunocytochemical neuronal labels, indicated the following: (1) Regenerating axons from the axotomized retinal ganglion cells extended along the entire PN grafts, covering a distance nearly twice that of the normal retinotectal projection of intact rats. (2) Some of these axons penetrated the SC and formed terminal arborizations up to 500 microns from the end of the graft. (3) By electron microscopy, the arborizations of these regenerated axons in the SC were seen as small HRP-labeled axonal profiles that contacted neuronal processes in the SC; some of these contacts showed pre- and postsynaptic membrane specializations. These findings indicate that injured retinal ganglion cells in the adult rat are not only able to regrow lengthy axons, but may also form synapses in the SC.

[1]  G. Bray,et al.  Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  S. Thanos,et al.  The use of rhodamine-B-isothiocyanate (RITC) as an anterograde and retrograde tracer in the adult rat visual system , 1987, Brain Research.

[3]  S. Carbonetto,et al.  Nerve fiber growth in culture on tissue substrata from central and peripheral nervous systems , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  F. Gage,et al.  Grafted septal neurons form cholinergic synaptic connections in the dentate gyrus of behaviorally impaired aged rats , 1986, The Journal of comparative neurology.

[5]  K. So,et al.  Effects on the growth of damaged ganglion cell axons after peripheral nerve transplantation in adult hamsters , 1986, Brain Research.

[6]  J. M. Hopkins,et al.  Laminin supports neurite outgrowth from explants of axotomized adult rat retinal neurons. , 1986, Brain research.

[7]  H. Clark,et al.  Induction of nerve growth factor receptor in Schwann cells after axotomy. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. Williams,et al.  Growth cones, dying axons, and developmental fluctuations in the fiber population of the cat's optic nerve , 1986, The Journal of comparative neurology.

[9]  E. Shooter,et al.  Expression of specific sheath cell proteins during peripheral nerve growth and regeneration in mammals , 1986, The Journal of cell biology.

[10]  P. Spencer,et al.  Regeneration of rat optic axons into peripheral nerve grafts , 1986, Experimental Neurology.

[11]  S. Keirstead,et al.  Responses to light of retinal neurons regenerating axons into peripheral nerve grafts in the rat , 1985, Brain Research.

[12]  S C McLoon,et al.  Evidence for shifting connections during development of the chick retinotectal projection , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  P. Liesi.  Laminin‐immunoreactive glia distinguish regenerative adult CNS systems from non‐regenerative ones. , 1985, The EMBO journal.

[14]  P. Rakić,et al.  Dispersion of growing axons within the optic nerve of the embryonic monkey. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[15]  A. Lander,et al.  Laminin is associated with the "neurite outgrowth-promoting factors" found in conditioned media. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[16]  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.

[17]  J. Powell,et al.  Efferent synaptic connections of grafted dopaminergic neurons reinnervating the host neostriatum: a tyrosine hydroxylase immunocytochemical study , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  J. A. Stevenson.  Growth of optic tract axons in nerve grafts in hamsters , 1985, Experimental Neurology.

[19]  C. Saper,et al.  Stabilization of TMB Reaction Product for electron microscopic retrograde and anterograde fiber tracing , 1985, Brain Research Bulletin.

[20]  M. Berry,et al.  A quantitative comparison of the reactions of retinal ganglion cells to optic nerve crush in neonatal and adult mice. , 1984, Brain research.

[21]  B. Wainer,et al.  Stabilization of the tetramethylbenzidine (TMB) reaction product: application for retrograde and anterograde tracing, and combination with immunohistochemistry. , 1984, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[22]  A. Gierer,et al.  How do retinal axons find their targets on the tectum? , 1984, Trends in Neurosciences.

[23]  U. Dräger,et al.  Antibodies to heavy neurofilament subunit detect a subpopulation of damaged ganglion cells in retina , 1984, Nature.

[24]  M. Murray,et al.  Viability of retinal ganglion cells after optic nerve crush in adult rats , 1984, Journal of neurocytology.

[25]  S. Cullheim,et al.  Reinnervation of the ventral root L7 from ventral horn neurons following intramedullary axotomy in adult cats , 1983, Brain Research.

[26]  S. Thanos,et al.  Investigations on the development and topographic order of retinotectal axons: Anterograde and retrograde staining of axons and perikarya with rhodamine in vivo , 1983, The Journal of comparative neurology.

[27]  P. Richardson,et al.  Regeneration and retrograde degeneration of axons in the rat optic nerve , 1982, Journal of neurocytology.

[28]  T. Ebendal,et al.  Nerve growth activities in rat peripheral nerve , 1982, Brain Research.

[29]  J. Ulrich,et al.  Monoclonal antibodies show that neurofibrillary tangles and neurofilaments share antigenic determinants , 1982, Nature.

[30]  R. Linden,et al.  Evidence for dendritic competition in the developing retina , 1982, Nature.

[31]  B. Grafstein,et al.  Intracranial transection of the optic nerve in adult mice: Preliminary observations , 1982, Experimental Neurology.

[32]  A. Aguayo,et al.  Extensive elongation of axons from rat brain into peripheral nerve grafts , 1982, Nature.

[33]  B. Dreher,et al.  The loss of ganglion cells in the developing retina of the rat. , 1982, Brain research.

[34]  V. Perry.  Evidence for an amacrine cell system in the ganglion cell layer of the rat retina , 1981, Neuroscience.

[35]  Hajime Fujisawa,et al.  Retinotopic analysis of fiber pathways in the regenerating retinotectal system of the adult newt cynops pyrrhogaster , 1981, Brain Research.

[36]  S. Goldberg,et al.  Will central nervous systems in the adult mammal regenerate after bypassing a lesion? A study in the mouse and chick visual systems , 1980, Experimental Neurology.

[37]  B. Grafstein,et al.  Early stages of axonal regeneration in the goldfish optic tract: An electron microscopic study , 1980, Journal of neurocytology.

[38]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[39]  J. Lund,et al.  Development of synaptic patterns in the superior colliculus of the rat. , 1972, Brain research.

[40]  A. Peters,et al.  Nerve Fibres in Optic Nerve of Rat , 1967, Nature.

[41]  L. Kruger,et al.  An electrophysiological study of the visual projection to the superior colliculus of the rat , 1966, The Journal of comparative neurology.

[42]  R. G. Janes,et al.  The blood vessels of the rat's eye. , 1955, The American journal of anatomy.

[43]  J. Eayrs.  Relationship between the Ganglion Cell Layer of the Retina and the Optic Nerve in the Rat * , 1952, The British journal of ophthalmology.

[44]  M. Berry,et al.  Regeneration of Axons in the Mammalian Visual System , 1986 .

[45]  L. McLoon,et al.  Visual system transplanted to the brain of rats , 1985 .

[46]  P. Patterson,et al.  The production of a monoclonal antibody that blocks the action of a neurite outgrowth-promoting factor. , 1983, Cold Spring Harbor symposia on quantitative biology.

[47]  H. Thoenen,et al.  New neurotrophic factors. , 1983, Annual review of physiology.

[48]  M. Berry,et al.  Regeneration of axons in the mouse retina after injury. , 1982, Bibliotheca anatomica.