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Role of cAMP Cascade in Synaptic Stability and Plasticity: Ultrastructural and Physiological Analyses of Individual Synaptic Boutons in Drosophila Memory Mutants

John J. Renger¹, Atsushi Ueda¹, Harold L. Atwood^{1, 2}, C. K. Govind³, and Chun-Fang Wu¹

¹ Department of Biological Sciences, University of Iowa, Iowa City, Iowa 52240, ² Department of Physiology, University of Toronto, Toronto, Ontario M5S 1A8, Canada, and ³ Life Sciences Division, Scarborough College, University of Toronto, Scarborough, Ontario M1C 1A4, Canada

Mutations of the genes rutabaga (rut) and dunce (dnc) affect the synthesis and degradation of cAMP, respectively, and disrupt learning in Drosophila. Combined ultrastructural analysis and focal electrophysiological recording in the larval neuromuscular junction revealed a loss of stability and fine tuning of synaptic structure and function in both mutants. Increased ratios of docked/undocked vesicles and poorly defined synaptic specializations characterized dnc synapses. In contrast, rut boutons possessed fewer, although larger, synapses with lower proportions of docked vesicles. At reduced Ca²⁺ levels, decreased quantal content coupled with an increase in failure rate was seen in rut boutons and reduced pair-pulse facilitation were found in both rut and dnc mutants. At physiological Ca²⁺ levels, strong enhancement, instead of depression, in evoked release was observed in some dnc and rut boutons during 10 Hz tetanus. Furthermore, increased variability of synaptic transmission, including fluctuation and asynchronicity of evoked release, paralleled an increase in synapse size variation in both dnc and rut boutons, which might impose problems for effective signal processing in the nervous system. Pharmacological and genetic studies indicated broader ranges of physiological alteration by dnc and rut mutations than either the acute effects of cAMP analogs or the available mutations that affect cAMP-dependent protein kinase (PKA) activity. This is consistent with previous reports of more severe learning defects in dnc and rut mutations than these PKA mutants and allows identification of the phenotypes involving long-term developmental regulation and those conferred by PKA.

Key words: Drosophila; synaptic ultrastructure; synaptic stability; variability and plasticity; neuromuscular junction; vesicle docking; learning and memory; dnc; rut; DCO; dPKA-RI

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Copyright © 2000 Society for Neuroscience  0270-6474/00/20113980-13$05.00/0

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