The Journal of Neuroscience, January 1, 2000, 20(1):361-374
Selective Innervation of Retinorecipient Brainstem Nuclei by
Retinal Ganglion Cell Axons Regenerating through Peripheral Nerve
Grafts in Adult Rats
Marcelino
Avilés-Trigueros1,
Yves
Sauvé2,
Raymond
D.
Lund2, and
Manuel
Vidal-Sanz1
1 Laboratorio de Oftalmología Experimental,
Departamento de Oftalmología, Facultad de Medicina, Universidad
de Murcia, E-30100 Espinardo, Murcia, Spain, and 2 Neural
Transplant Program, Department of Pathology, Institute of
Ophthalmology, London EC1V 9EL, UK
The pattern of axonal regeneration, specificity of reinnervation,
and terminal arborization in the brainstem by axotomized retinal
ganglion cell axons was studied in rats with peripheral nerve grafts
linking the retina with ipsilateral regions of the brainstem, including
dorsal and lateral aspects of the diencephalon and lateral aspect of
the superior colliculus. Four to 13 months later, regenerated retinal
projections were traced using intraocular injection of cholera toxin B
subunit. In approximately one-third of the animals, regenerated retinal
axons extended into the brainstem for distances of up to 6 mm. Although
axons followed different patterns of ingrowth depending on their site
of entry to the brainstem, within the pretectum, they innervated
preferentially the nucleus of the optic tract and the olivary pretectal
nucleus in which they formed two types of terminal arbors. Within the
superior colliculus, axons extended laterally and formed a different
terminal arbor type within the stratum griseum superficiale. In the
remaining two-thirds of the animals, retinal fibers formed a
neuroma-like structure at the site of entry into the brainstem, or a
few fibers extended for very short distances within the neighboring
neuropil. These experiments suggest that regenerated retinal axons are
capable of a highly selective reinnervation pattern within adult
denervated retinorecipient nuclei in which they form well
defined terminal arbors that may persist for long periods of time. In
addition, these studies provide the anatomical correlate for our
previous functional study on the re-establishment of the pupillary
light reflex in this experimental paradigm.
Key words:
peripheral nerve; axonal regeneration; retina; pretectal
nuclei; superior colliculus; adult mammal
Copyright © 2000 Society for Neuroscience 0270-6474/0/201361-14$05.00/0