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Journal of Neuroscience, Vol 16, 1101-1113, Copyright © 1996 by Society for Neuroscience
Mutations in shaking-B prevent electrical synapse formation in the Drosophila giant fiber system
P Phelan, M Nakagawa, MB Wilkin, KG Moffat, CJ O'Kane, JA Davies and JP Bacon
Sussex Centre for Neuroscience, School of Biological Sciences, University of Sussex, Brighton, United Kingdom.
The giant fiber system (GFS) is a simple network of neurons that mediates
visually elicited escape behavior in Drosophila. The giant fiber (GF), the
major component of the system, is a large, descending interneuron that
relays visual stimuli to the motoneurons that innervate the
tergotrochanteral jump muscle (TTM) and dorsal longitudinal flight muscles
(DLMs). Mutations in the neural transcript from the shaking-B locus abolish
the behavioral response by disrupting transmission at some electrical
synapses in the GFS. This study focuses on the role of the gene in the
development of the synaptic connections. Using an enhancer-trap line that
expresses lacZ in the GFs, we show that the neurons develop during the
first 30 hr of metamorphosis. Within the next 15 hr, they begin to form
electrical synapses, as indicated by the transfer of intracellularly
injected Lucifer yellow. The GFs dye-couple to the TTM motoneuron between
30 and 45 hr of metamorphosis, to the peripherally synapsing interneuron
that drives the DLM motoneurons at approximately 48 hr, and to giant
commissural interneurons in the brain at approximately 55 hr.
Immunocytochemistry with shaking-B peptide antisera demonstrates that the
expression of shaking-B protein in the region of GFS synapses coincides
temporally with the onset of synaptogenesis; expression persists
thereafter. The mutation shak-B2, which eliminates protein expression,
prevents the establishment of dye coupling shaking-B, therefore, is
essential for the assembly and/or maintenance of functional gap junctions
at electrical synapses in the GFS.
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