Alternate neuromuscular target selection following the loss of single muscle fibers in Drosophila

Abstract

The Drosophila embryonic and larval body wall consists of a simple array of segmental muscle fibers, innervated in a precise manner by identified neurons. During development motoneurons were forced to find alternate targets following the selective deletion of a single muscle fiber, the pleural internal oblique #5. We used backfills, intracellular dyefills, and immunocytochemistry in embryos and larvae to characterize the normal motoneurons to the fiber. Deleting the fiber using either a genetic or laser lesioning method yielded essentially the same result. In nearly half the cases examined, an ectopically placed neuromuscular projection was found on either of two neighboring muscle fibers, with one favored eight times more than the other. The ectopic projection derived from the nerve branch that normally supplied the deleted muscle fiber 5. Motoneuronal endings on undeleted muscle fibers elsewhere in the body wall had normal morphology. The ectopically placed motor terminals accumulated glutamate in normally sized synaptic boutons, beneath which transmitter sensitivity was localized. The number of boutons and branches at the ectopic endings did not differ significantly from those on intact muscle fiber 5s. Also, the native motoneurons did not alter their arborization sizes in response to a supernumerary ectopically placed contact. While the orientation of the individual ectopically placed branches was variable, the ectopic endings occupied a predictable site on the surrogate muscle fibers. The results suggest that Drosophila motoneurons can project to body wall destinations in the absence of their muscle fiber targets, and that alternate muscle fibers are selected by their proximity. The muscle fibers will support apparently stable and functional supernumerary motor endings on ectopic sites, and these inputs do not significantly influence the behavior of the native motoneurons. The data suggest that Drosophila motoneurons may behave autonomously when making synapses, and that competition does not play a major role in the matching of motoneuron to muscle fiber.