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Journal of Neuroscience, Vol 9, 710-725, Copyright © 1989 by Society for Neuroscience
Stereotypic morphology of glutamatergic synapses on identified muscle cells of Drosophila larvae
J Johansen, ME Halpern, KM Johansen and H Keshishian
Department of Biology, Yale University, New Haven, Connecticut 06511.
The distribution and morphology of glutamatergic synapses on Drosophila
bodywall muscle fibers were examined at the single-synapse level using
immunocytochemistry and electrophysiology. We find that glutamate-
immunoreactive motor endings innervate the entire larval bodywall
musculature, with each muscle fiber receiving at least one glutamatergic
ending. The innervation is initiated at stereotyped locations on each
muscle fiber from where moderately branched varicose nerve processes
project over the internally facing muscle surface. Individual muscle fibers
have distinct stereotypic patterns of nerve endings that occupy
characteristic regions on the cell surface. The muscle-specific branching
pattern of motor endings is reiterated by segmentally homologous fibers.
Two morphological types of innervating nerve processes can be distinguished
by their bouton size distributions: (1) Type I processes, which have
localized branching and a broad size distribution of relatively large
varicosities ranging up to 8 microns (mean diameter, 3.1 +/- 1.6 microns;
+/- SD, n = 521), and (2) thinner Type II processes, which have a narrower
distribution of small varicosities with a mean diameter of only 1.4 +/- 0.6
microns (+/- SD, n = 214). Immunoelectron microscopy with
peroxidase-labeled second antibody demonstrates that the varicosities are
surrounded by a subsynaptic reticulum, that they contain immunoreactive
vesicles of about 30-50 nm, and thus probably represent synaptic release
sites. By iontophoretic application of glutamate we mapped the responsive
sites on the muscle surface and found an excellent correspondence between
transmitter sensitivity and the patterns of endings as described by
immunocytochemistry. In contrast to our finding of numerous glutamate
iontophoresis-sensitive sites, we did not detect any aspartate- responsive
muscles. These data provide strong new evidence for glutamate being an
endogenous transmitter at the Drosophila larval neuromuscular junction.
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