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Journal of Neuroscience, Vol 13, 144-166, Copyright © 1993 by Society for Neuroscience
Development of the embryonic neuromuscular synapse of Drosophila melanogaster
KS Broadie and M Bate
Department of Zoology, University of Cambridge, United Kingdom.
We have examined the embryonic development of an identified neuromuscular
junction (NMJ) of Drosophila melanogaster using whole- cell patch-clamp and
a variety of physiological and morphological techniques. Synaptic current
at the embryonic NMJ is carried through a large-conductance (200 pS)
L-glutamate receptor. Early synaptic communication is characterized by
frequent, brief (< 10 msec) currents carried through few (1-10)
receptors and relatively rare, prolonged currents (up to seconds) of
similar amplitude. The brief currents have a time course similar to the
mature larval excitatory junction currents (EJCs), but the prolonged
currents are restricted to early stages of synaptogenesis. The amplitude of
EJCs rapidly increases, and the frequency of the prolonged currents
decreases, after the initial stages of synaptogenesis. Early prolonged
(seconds), nonspiking synaptic potentials are replaced with rapid (<
0.10 sec), spiking synaptic potentials later in development. The early
synapse appears tenuous, easily fatiguable, and with inconsistent
communication properties. Synaptogenesis can be divided into a sequence of
progressive stages. (1) Motor axon filopodia begin neurotransmitter
expression and concurrent exploration of the myotube surface. (2) Myotubes
uncouple to form single-cell units soon after motor axon contact. (3) A
small number of transmitter receptors are homogeneously displayed on the
myotube surface immediately following myotube uncoupling. (4) Endogenous
transmitter release from pioneering growth cones is detected; nerve
stimulation elicits postsynaptic EJC response. (5) Motor axon filopodia and
transmitter receptors are localized to the mature synaptic zone; filopodial
localization is complete in advance of receptor localization. (6) A
functional neuromuscular synapse is formed; endogenous muscular activity
begins; nerve stimulation leads to muscle contraction. (7) Morphological
presynaptic specializations develop; synapse develops mature morphology.
(8) A second motor axon synapses on the myotube at the pre-established
synaptic zone. (9) Vigorous neuromuscular activity, characteristic of
larval locomotory movements, begins. (10) A second stage of receptor
expression begins and continues through the end of embryogenesis. In
general, Drosophila neuromuscular synaptogenesis appears similar to
neuromuscular synaptogenesis in known vertebrate preparations. We suggest
that this system provides a model for synaptogenesis in which investigation
can be readily extended to a genetic and molecular level.
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