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Journal of Neuroscience, Vol 9, 4318-4332, Copyright © 1989 by Society for Neuroscience
Axonal guidance and the development of muscle fiber-specific innervation in Drosophila embryos
J Johansen, ME Halpern and H Keshishian
Department of Biology, Yale University, New Haven, Connecticut 06511.
The outgrowth of peripheral nerves and the development of muscle fiber-
specific neuromuscular junctions were examined in Drosophila embryos using
immunocytochemistry and computer-enhanced digital optical microscopy. We
find that the pioneering of the peripheral nerves and the formation of the
neuromuscular junctions occur through a precisely orchestrated sequence of
stereotyped axonal trajectories, mediated by the selective growth cone
choices of pioneer motoneurons. We have also examined the establishment of
the embryonic muscle fibers and, using intracellular dye fills, have
identified cells that are putative muscle pioneers. The muscle fibers of
the bodywall have completed their morphogenesis prior to the initiation of
synaptic contacts, and owing to the timing of neurite outgrowth from the
CNS, synaptogenesis is synchronous at muscle fibers throughout the
bodywall. At each muscle fiber the innervating axons make their initial
contacts on a characteristic surface domain of the target cell's membrane.
Through stereotyped growth cone-mediated trajectories the motoneurons
actively establish the basic anatomical features of the mature
neuromuscular junction, including the stereotyped, muscle fiber-specific
branch anatomy. These events occur without significant process pruning or
apparent synapse elimination. Our results suggest that the basic elements
of the mature neuromuscular innervation, including the details of the
ending trajectory on the target cell's surface, are formed by the precise
navigation and presumed recognition by the motoneuron growth cones of
muscle membrane surface features.
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