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Journal of Neuroscience, Vol 13, 714-732, Copyright © 1993 by Society for Neuroscience
Growth cone choices of Drosophila motoneurons in response to muscle fiber mismatch
A Chiba, H Hing, S Cash and H Keshishian
Department of Biology, Yale University, New Haven, Connecticut 06511.
In Drosophila embryos, each motoneuron is accurately matched to one or more
singly identifiable muscle fibers. In this article we altered the number
and pattern of the embryonic muscle fibers using genetic, heat shock, and
laser ablation methods to test whether motoneuron growth cones are able to
recognize specific targets. The choices made by two motoneurons were
assayed using both intracellular dye fills and immunocytochemistry. The
motoneurons RP1 and RP3 have nearly identical central and peripheral axonal
trajectories. However, RP3 innervates the two most ventral longitudinal
muscle fibers, 7 and 6, while RP1 grows past these fibers to innervate only
muscle fiber 13. In rhomboid mutants muscle fiber 7 does not develop.
Despite the loss of one of its targets, RP3 faithfully innervated the
remaining muscle fiber 6 in over 80% of the observed cases. Furthermore,
neuron RP1 accurately innervated muscle fiber 13, although it traversed one
fiber fewer to reach it. Laser ablation of muscle fiber 7 confirmed the
target choices shown by the motoneurons. In numb mutants, multiple muscle
fibers, including 7, 13, and 12, fail to develop. This allowed us to test
whether fibers distal to the target are involved in muscle fiber
recognition, possibly by halting the growth cone advance. In mutant
embryos, RP3 innervated muscle fiber 6 at the same frequency regardless of
the absence of the distal muscle fiber 13. By contrast, RP1, which had lost
its target entirely, frequently failed to innervate any muscle fiber during
the period examined. Finally, muscle fiber 13 can be duplicated in
wild-type embryos by means of a brief heat pulse during myogenesis.
Presented with two targets, RP1 innervated both fibers in each case
examined, while RP3 synapsed with muscle fibers 7 and 6 normally.
Neuron-specific antibodies revealed that the embryonic growth cone choices
were not transient, but persisted into the larval neuromuscular
projections. These results indicate that each motoneuron growth cone has a
primary target preference, which is retained even when the numbers of the
muscle fibers, and therefore their relative positions, are altered. We
therefore suggest that synaptic recognition by Drosophila motoneuron growth
cones relies on unique features of the individual muscle fibers.
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