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Previous Article
Journal of Neuroscience, Vol 10, 3754-3768, Copyright © 1990 by Society for Neuroscience
Morphological plasticity of motor axons in Drosophila mutants with altered excitability
V Budnik, Y Zhong and CF Wu
Department of Biology, University of Iowa, Iowa City 52242.
An anatomical and electrophysiological study of Drosophila mutants has been
made to determine the effect of altered electrical activity on the
development and maintenance of larval neuromuscular junctions. We examined
motor axon terminals of (1) hyperexcitable mutants Shaker (Sh), ether a
go-go (eag), Hyperkinetic (Hk), and Duplication of para+ (Dp para+); and
(2) mutants with reduced excitability, no action potential (napts) and
paralytic (parats 1). Nerve terminals innervating larval body-wall muscles
were visualized by using anti-HRP immunocytochemistry, which specifically
stains neurons in insect species. In wild-type larvae, motor axon terminals
were distributed in a stereotypic fashion. However, in combinations of eag
and Sh alleles, the basic pattern of innervation was altered. There was an
increase in both the number of higher-order axonal branches over the
muscles and the number of varicosities on the neurites. A similar
phenomenon was found in the double mutant Hk eag and, to a lesser extent,
in Dp para+ and Dp para+ Sh mutants. It is known that at permissive
temperature the napts, but not parats 1, mutation decreases excitability of
larval motor axons and suppresses the behavioral phenotypes of Sh, eag, and
Hk. In the mutant napts (reared at permissive temperature), a slight
decrease in the extent of branching was observed. Yet, when combined with
eag Sh, napts completely reversed the morphological abnormality in eag Sh
mutants. No such reversion was observed in parats 1 eag Sh mutants. The
endogenous patterns of electrical activity at the neuromuscular junction
were analyzed by extracellular recordings in a semi-intact larval
preparation. Recordings from wild-type body-wall muscles revealed rhythmic
bursts of spikes. In eag Sh mutants, this rhythmic activity was accompanied
by or superimposed on periods of strong tonic activity. This abnormal
pattern of activity could be partially suppressed by napts in combination
with eag Sh.
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|
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