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Journal of Neuroscience, Vol 12, 1212-1232, Copyright © 1992 by Society for Neuroscience
Development of topographic order in the mammalian retinocollicular projection
DK Simon and DD O'Leary
Molecular Neurobiology Laboratory, Salk Institute, La Jolla, California 92037.
We have used the anterograde axon tracer 1,1'-dioctodecyl-3,3,3',3'-
tetramethylindocarbocyanine perchlorate (Dil) to characterize the
development of topographic order in the rat retinocollicular projection.
Retinal axons were labeled by Dil injections covering 0.15- 2% of
peripheral temporal, nasal, superior, or inferior retina, or more central
retina, in rats ranging in age from embryonic day 20 to postnatal day (P)
19. At P11-P12 and later, such injections label retinal axons that form
overlapping arbors restricted to a topographically correct terminal zone
covering about 1% of the superior colliculus (SC) area. At perinatal ages,
though, axons labeled from each retinal site are distributed in the SC over
much of its medial- lateral axis and extend caudally well beyond the
rostral-caudal location of their correct terminal zone; some continue
caudally into the inferior colliculus. Axons typically form side branches
and often arborize at topographically incorrect positions throughout the
SC; however, they appear to branch preferentially in a region that
includes, but is much larger than, their correct terminal zone. The mature,
retinotopically ordered projection emerges during an early postnatal
remodeling period through the rapid remodeling of the early, diffuse
projection. This process involves the large-scale removal of axons, axon
segments, branches, and arbors from topographically inappropriate positions
concurrently with a dramatic increase in branching and arborization at
topographically correct locations. Quantitative measurements show that
elimination of aberrant branches without loss of the primary axons
contributes substantially to the development of order. By P6, fewer
mistargeted axons persist, but those that do persist tend to branch or
arborize more extensively in topographically inappropriate regions. By P8,
the labeling patterns begin to approximate those seen at maturity. Further
refinement leads to an adultlike topographic ordering of axonal
arborizations by P11- P12. At maturity, some axons take very indirect
routes to reach their correct terminal zone. However, such trajectory
changes typically correct only small positional inaccuracies, indicating
that axons and axon segments that make larger targeting errors do not
survive the remodeling phase. Previous retrograde labeling studies indicate
that some retinal axons make topographic targeting errors (O'Leary et al.,
1986; Yhip and Kirby, 1990), but none have suggested the degree of
diffuseness revealed by anterograde labeling with Dil. Our findings show
that directed axon growth is inadequate as a mechanism to develop the
topographic ordering of retinal axons in the rat SC. Rather, mechanisms
that control the removal of mistargeted axons and promote the arborization
of correctly positioned axons are critical for the development of
retinotopic order.(ABSTRACT TRUNCATED AT 400 WORDS)
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