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Journal of Neuroscience, Vol 9, 3776-3795, Copyright © 1989 by Society for Neuroscience
Inaccuracies in initial growth and arborization of chick retinotectal axons followed by course corrections and axon remodeling to develop topographic order
H Nakamura and DD O'Leary
Department of Anatomy, Washington University School of Medicine, St. Louis, Missouri 63110.
The retinotectal projection is organized in a precise retinotopic manner.
We find, though, that during development the growth and arborization of
temporal retinal axons within the optic tectum of chick embryos is
initially imprecise. Axonal targeting errors occur along the rostral-caudal
and medial-lateral tectal axes, and arbors are formed at topographically
inappropriate positions. Subsequent course corrections along both tectal
axes and large-scale axonal remodeling lead to the retinotopic ordering of
terminal arborizations characteristic of the mature projection. The
trajectories and branching patterns of temporal retinal axons labeled with
Dil or DiO were determined in whole mounts of retina and tectum from chicks
ranging in age from embryonic day 9 to posthatching. Within the retina,
labeled retinofugal axons travel in a compact bundle but do not maintain
strict neighbor relations, as they course to the optic fissure. The axons
enter the contralateral tectum at its rostral edge and grow caudally. Many
extend well past their appropriate terminal zone within rostral tectum; a
proportion of these later reverse their direction of growth. Many axons
grow onto the tectum at incorrect positions along the medial-lateral tectal
axis. Some correct this error in a directed manner by altering their
trajectory or extending collateral branches at right angles. About 80% of
the positional changes of this type are made in the direction appropriate
to correct axon position, and thus are likely a response to tectal
positional cues. After maturation of retinotopic order, about half of the
axons that project to a mature terminal zone have made abrupt course
corrections along one or both tectal axes, indicating that initially
mistargeted axons can establish appropriately positioned arbors and
survive. The development of temporal axons within the tectum is
characterized by 3 phases: elongation, branch and arbor formation, and
remodeling. After considerable rostrocaudal elongation, an axon typically
develops numerous side branches and arbors, many at inappropriate
locations. Most arbors are formed by side branches that develop as
interstitial collaterals; few axons grow directly to their appropriate
terminal zone and arborize. Aberrant arbors, and axons and axon segments
that fail to form arbors in the appropriate terminal zone, are rapidly
eliminated over about a 2 d period. Axon degeneration appears to play a
role in this remodeling process.
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