Journal of Neuroscience, Vol 11, 1081-1094, Copyright © 1991 by Society for Neuroscience
Growth cone distribution patterns in the optic nerve of fetal monkeys: implications for mechanisms of axon guidance
RW Williams, M Borodkin and P Rakic
Section of Neuroanatomy, Yale University School of Medicine, New Haven, Connecticut 06510.
The distribution of growth cones was studied in the optic nerve of monkeys
during the first half of prenatal development using quantitative electron
microscopic methods. Our aim was to test the hypothesis that ganglion cell
growth cones extend predominantly along the surfaces of the nerve, just
beneath the pia mater. A complete census of growth cones in cross sections
of the nerve during the early phase of axon ingrowth, from embryonic day 39
(E39) to E41, demonstrates that growth cones are scattered within the
majority of fascicles, even those located far from the surface of the
nerve. By E45, growth cones are concentrated around the nasal, dorsal, and
ventral edge of the optic nerve. They are less concentrated in the core and
around the temporal edge. However, even as late as E49, virtually all
fascicles in the nerve, whether deep or superficial, contain growth cones.
Growth cones are dispersed within single fascicles and are often located
far from glia. Thus, the newest fibers penetrate deep parts of the pathway
and push through centers of densely packed bundles of older axons. This
finding is consistent with the vagrant paths of growing axons reported in
previous work on embryonic monkey optic nerve (Williams and Rakic, 1985).
Our data challenge the hypotheses that growth cones extend selectively
along the basal lamina, the pia mater, or glial end feet. Gradients found
at later stages of development in the nerve are not due to a particular
affinity of growth cones for non- neuronal substrata. The pattern we
observed is much more likely to result from central-to-peripheral gradients
in ganglion cell generation and possible associations between growth cones
originating from the same regions of the retina.
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