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Journal of Neuroscience, Vol 9, 3123-3145, Copyright © 1989 by Society for Neuroscience
A single-cell analysis of early retinal ganglion cell differentiation in Xenopus: from soma to axon tip
CE Holt
Department of Biology, University of California, San Diego, La Jolla 92093.
Intracellular injections of Lucifer yellow (LY) were made into the cell
bodies of Xenopus retinal ganglion cells from the earliest stages of
axonogenesis to the beginning of target innervation. Embryos were intact
during the injection so that the entire cell (cell body, dendrites, axon,
and growth cone) could be visualized. The purpose of the study was 3-fold:
(1) to characterize the early steps in retinal ganglion cell
differentiation before the axon reaches its target; (2) to determine
whether guidepost cells exist as possible navigation cues in the vertebrate
optic pathway; and (3) to investigate whether the morphology of early
retinal ganglion cell growth cones varies in a position-dependent manner
along the primordial optic pathway. Axons were generally initiated before
dendrites and followed a well-defined course along the primordial optic
pathway without branching. Surprisingly, at least 5% of the retinal
ganglion cells sent more than one axon into the optic pathway. Sister axons
from the same parent cell traveled separately in the pathway, indicating
that their growth cones navigated independently. Examination of dendrite
genesis showed that dendrites usually begin to emerge from the cell body
well before the axon tip reaches the target. This observation argues
against the possibility that target contact influences dendrite initiation.
Nascent dendrites were commonly tipped with pronounced varicosities that
did not resemble axon growth cones. Their number and branching correlated
well with axon length, indicating that the age of the retinal ganglion cell
itself, rather than the age of its presynaptic cells or local environment,
is the strongest influence on dendrite genesis. Examination of LY-filled
growth cones at varying points in the pathway showed no evidence of dye
transfer to adjacent cells. This indicates that gap junctional contacts
probably do not form during axonal pathfinding and suggests that direct
intercellular communication between growing axons and other cells in the
pathway does not play a major role in axon guidance. Growth cone morphology
was analyzed quantitatively and found to vary at different positions along
the pathway. Growth cones entering the optic nerve head were the largest
and most complex; those on the retinal surface were the smallest and showed
a simple morphology. Growth cones in the chiasm and optic tract showed a
degree of complexity similar to those in the optic nerve head but were
smaller.(ABSTRACT TRUNCATED AT 400 WORDS)
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