Role of rut adenylyl cyclase in the ensemble regulation of presynaptic terminal excitability: reduced synaptic strength and precision in a Drosophila memory mutant

Atsushi Ueda; Chun-Fang Wu

doi:10.1080/01677060802471726

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Role of rut adenylyl cyclase in the ensemble regulation of presynaptic terminal excitability: reduced synaptic strength and precision in a Drosophila memory mutant

Journal article

Peer reviewed

Role of rut adenylyl cyclase in the ensemble regulation of presynaptic terminal excitability: reduced synaptic strength and precision in a Drosophila memory mutant

Atsushi Ueda and Chun-Fang Wu

Journal of neurogenetics, Vol.23(1-2), pp.185-199

2009

DOI: 10.1080/01677060802471726

PMCID: PMC2743603

PMID: 19101836

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Abstract

Although modulation of presynaptic terminal excitability can profoundly affect transmission efficacy, how excitability along axonal terminal branches is regulated requires further investigations. We performed focal patch recording in Drosophila larval neuromuscular junctions (NMJs) to monitor the activity of individual synaptic boutons along the presynaptic terminal. Analysis of the learning mutant rutabaga (rut) suggests a tight regulation of presynaptic terminal excitability by rut adenylyl cyclase (AC) that is responsible for Ca2+/calmodulin-dependent cAMP synthesis. Focal excitatory junctional currents (ejcs) demonstrated that disrupted cAMP metabolism in rut mutant boutons leads to decreased transmitter release, coupled with temporal dispersion and amplitude fluctuation of ejcs during repetitive activity. Strikingly, rut motor terminals displayed greatly increased variability among corresponding terminal branches of identified NMJs in different preparations. However, boutons throughout single terminal branches were relatively uniform in either WT or rut mutant larvae. The use of electrotonic depolarization to directly evoke transmitter release from axonal terminals revealed that variability in neurotransmission originated from varying degrees of weakened excitability in rut terminals. Pharmacological treatments and axonal action potential recordings raised the possibility that defective rut AC resulted in reduced Ca2+ currents in the nerve terminal. Thus, our data indicate that rut AC not only affects transmitter release machinery, but also plays a previously unsuspected role in local excitability control, both contributing to transmission level and precision along the entire axonal terminal.

Drosophila melanogaster - physiology

Synaptic Transmission - physiology

Calcium - metabolism

Adenylyl Cyclases - physiology

Presynaptic Terminals - physiology

Action Potentials - physiology

Cyclic AMP - physiology

Calcium Channels - physiology

Drosophila Proteins - physiology

Patch-Clamp Techniques

Animals

Neuronal Plasticity - physiology

Mutation

Sodium - physiology

Memory - physiology

Neuromuscular Junction - physiology

Details

Title: Subtitle: Role of rut adenylyl cyclase in the ensemble regulation of presynaptic terminal excitability: reduced synaptic strength and precision in a Drosophila memory mutant
Creators: Atsushi Ueda - Department of Biological Sciences, University of Iowa, Iowa City, Iowa 52242, USA
Chun-Fang Wu
Resource Type: Journal article
Publication Details: Journal of neurogenetics, Vol.23(1-2), pp.185-199
DOI: 10.1080/01677060802471726
PMID: 19101836
PMCID: PMC2743603
NLM abbreviation: J Neurogenet
ISSN: 0167-7063
eISSN: 1563-5260
Publisher: Informa UK Limited; England
Grant note: R01 NS026528 / NINDS NIH HHS\nHD18577 / NICHD NIH HHS\nR01 NS026528-17 / NINDS NIH HHS\nP01 HD018577-220003 / NICHD NIH HHS\nNS26528 / NINDS NIH HHS\nP01 HD018577-210003 / NICHD NIH HHS\nR01 NS026528-16 / NINDS NIH HHS\nP01 HD018577 / NICHD NIH HHS
Language: English
Date published: 2009
Academic Unit: Iowa Neuroscience Institute; Biology
Record Identifier: 9984070253402771

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