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Journal of Neuroscience, Vol 11, 3227-3238, Copyright © 1991 by Society for Neuroscience
Growth cone behavior underlying the development of stereotypic synaptic connections in Drosophila embryos
ME Halpern, A Chiba, J Johansen and H Keshishian
Department of Biology, Yale University, New Haven, Connecticut 06511.
Each muscle fiber in the segmented body wall of Drosophila larvae is
innervated by anatomically stereotyped neuromuscular junctions. These
synapses arise through the selective choices of motoneuronal growth cones
at their peripheral targets. Using digital optical microscopy of staged
intracellular dye fills, we have singly identified embryonic motoneurons
and have examined individual growth cones when they contact and
differentiate at the target cells. There is a precise connectivity between
motoneuron and muscle fiber, which is the direct consequence of growth cone
behavior. We have also found that Drosophila muscle fibers possess
molecularly heterogeneous cell surfaces that may be involved in growth cone
recognition of appropriate targets. Fasciclin III, a homophilic adhesion
molecule, is coexpressed by several of the efferent growth cones and in a
site-specific fashion by the target muscle fiber's membrane. The fasciclin
III expression is transient, corresponding to the period in embryogenesis
when the first neuromuscular contacts are made. Upon encountering the
target cell surface, the growth cones can sprout stereotypically arrayed
filopodial processes, orient along the anterior-posterior axis, and turn in
predictable directions. Subsequently, terminal branches are established in
a nonrandom order. These phenomena were found to occur in two motoneurons
that innervate adjacent muscle fiber targets, and may be general features
of neuromuscular synaptogenesis in Drosophila.
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